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Sex Differentiation Begins During Early Development

By Claire Asher, on 27 August 2014

Males and females look different from each other, and these sexual dimorphisms are the result, largely, of sex differences in the expression of certain genes. Typically, scientists have studied sexual dimorphism in sexually mature adult animals, as this is the lifestage where differences are most apparent. However, many sex-specific phenotypes arise from sex-biased development, so sex-biased gene expression should be expected to begin during development. Recent research from GEE reveals complex patterns of sex- and stage-dependent gene expression, resulting from differing evolutionary pressures on difference sexes. In fact, sex-biased gene expression is actually most evident during early development.

Although there are some genetic differences between males and females, found on the sex chromosomes (Y in mammals, W in Birds), these contribute relatively little to the physical and behavioural differences between the sexes. Further, some animals (such as many reptiles) don’t possess a sex chromosome at all, instead determining sex based on environmental factors such as temperature. Scientists therefore believe that the majority of sexually dimorphic characteristics are generated from differences in the expression patterns of a shared set of genes, and there is now plenty of evidence for this in a variety of different species. In fact, sexual phenotypes appear to exist along a continuum, with some individuals in certain species exhibiting intermediate traits (e.g. subordinate male Turkeys).

The fruit fly,
Drosophila melanogaster

In most species, sex differences are less apparent during development and appear or become more pronounced at the onset of sexual maturity. This makes sense, since that’s generally when the sex-specific traits are useful. Nevertheless, the groundwork for producing these traits in adulthood must be laid during development, so we might expect to see sex-biased gene expression in juveniles as well. A recent paper by GEE academics Professor Judith Mank and Dr Peter Harrison, and Dr Jennifer Perry (University of Oxford) investigated gene expression patterns during larval development in the fruit fly, Drosophila melanogaster.

Juveniles Show Sex-Biased Gene Expression

The authors compared gene expression patterns in pre-gonad tissue in larvae and pre-pupae with gonad tissue in adult flies. Using transcriptome sequencing, which sequences all expressed genes, they were able to detect differences in gene expression between sexes at different developmental stages. By using a single tissue, the authors hoped to gain a clearer picture of gene expression in relation to sex and development, as tissue-specific gene expression can cloud the picture. Gonad and pre-gonad tissue was the obvious candidate, since this tissue forms sperm and eggs and is therefore likely to be under strong selection for sex-biased gene expression.

Despite the long-running assumption that sex-biased gene expression should not be prevalent in juveniles, the results of this study indicated that most genes show sex-bias in at least one pre-adult stage! Over 50% of genes showed at least 2-fold differences in gene expression between the sexes during larval or pre-pupae developmental stages. Sex was still the most important factor, however, with individuals within a sex showing greater similarity in gene expression patterns than individuals within a developmental stage.

. Venn diagrams of the number and percentage of genes showing sex-biased gene expression in larvae, pre-pupae, and adults. Image from open access article.

Venn diagrams of the number and percentage of genes showing sex-biased gene expression in larvae, pre-pupae, and adults. Image from open access article.

Continuity and Sex Differences

The majority of sex-biased genes showed expression patterns that remained consistent throughout development, however a significant minority (~25%) of genes showed varying sex-bias according to developmental stage. For example, a gene that showed lower expression in females during the larval stage might then show higher expression in females during adulthood.

In the majority of previous studies have found that more genes show male-bias in adults. By contrast, this study showed that in larval and pre-pupal stages of development in Drosophila melanogaster, more genes show female-biased gene expression. Females were also more likely to show stage-dependent sex-biases in gene expression. The exception to this was genes showing very extreme sex-bias, which tended to be male-biased. This is consistent with the finding that the overall magnitude of gene expression differences tended to be higher in male-biased genes.

The Rate and Form of Evolution

The authors then investigated the evolutionary dynamics that lead to these patterns of gene expression. Genes showing the most rapid recent evolution were those that showed male-biased expression continously throughout life, and those that showed female-biased expression in the larval stages. The evolutionary pressures in male- and female-biased genes were different for each sex. For female-biased genes expressed in larvae, rapid evolution was the result of a relaxation of purifying selection for stage-dependent genes (natural selection that removes harmful mutations), whereas rapid evolution in consistently male-biased genes was a result of stronger purifying selection on stage-dependent genes.

This study reveals complex and intricate relationships between sex, age, development and gene expression in the fruit fly, Drosophila melanogaster. Despite minimal visible differences between the sexes during larval and pre-pupal development, there were vast differences in terms of gene expression. Although this is contrary to previous assumptions about the nature of sex-biased gene expression, it is consistent with the fact that many sexually dimorphic traits exhibited by adults must by necessity begin to develop before adulthood. It is therefore not surprising that sex-biased gene expression is evident in juveniles, however the extent of this bias is quite a surprise. More research is needed to understand the evolutionary dynamics shaping development- and sex-specific gene expression, and how these patterns vary across different tissue types.

Original Article:

() The Ontogeny and Evolution of Sex-Biased Gene Expression in Drosophila melanogaster Molecular Biology and Evolution

Further Reading:

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This research was made possible by funding from the European Research Council (ERC), the Elizabeth Hannah Jenkinson Fund and the John Fell Oxford University Press Research Fund

Extinction and Species Declines:
Defaunation in the Anthropocene

By Claire Asher, on 18 August 2014

We are in the grips of a mass extinction. There have been mass extinctions throughout evolutionary history, what makes this one different is that we’re the ones causing it. A recent review paper from GEE’s Dr Ben Collen discusses the current loss of biodiversity and suggests that our main concerns are species and population declines, which alter ecosystem dynamics and threaten our food, water and health. Understanding the drivers of local declines is more complex than understanding species extinction, but may be more pertinent to our ongoing health and survival.

The history of life on Earth has been punctuated by five mass-extinction events; from the Ordovician-Silurian extinction that killed 85% of sea life 443 million years ago, to the famous Cretaceous-Tertiary extinction that wiped out the dinosaurs 65 million years ago, mass extinctions have been a part of life. However, we are now in the middle of the sixth mass extinction event, and we’re the ones who are causing it. The last 500 years has seen humans cause a wave of extinctions of such speed and magnitude that it rivals the big five extinction events of the past.

Defaunation in the Anthropocene

Like other mass extinctions, the Anthropocene extinction event is affecting all taxonomic groups, although some are being hit harder than others. Since 1500, over 300 terrestrial vertebrates, 90 fish and nearly 400 are known to have been driven to extinction (although the real figures are likely much higher!). A conservative estimate suggests that we may be losing anywhere between 10,000 and 60,000 species each year. Many of these species go extinct before we ever even get a chance to identify them. Extinction is not evenly distributed, though – amphibians appear to be worse affected than birds, for example. Perhaps more worrying, many remaining species are suffering severe population declines. Globally, terrestrial vertebrate populations show declines of 25%, and 67% of monitored invertebrate populations are declining by 45%! The loss of species from ecosystems, either through local population declines or species extinction, will undoubtedly disrupt ecosystem function and the key ecosystem services humans rely on for survival and well being.

Scientists have coined the term ‘defaunation’ to include the extinction of species and populations as well as local declines in abundance. Defaunation can be thought of as deforestation for animals. It is an important point to make that although species extinctions are conspicuous and striking, the real damage to ecosystem function happens a long time before the final extinction event. Declines in populations will alter community composition far more than the final loss of the few remaining individuals of a population, and further, population declines have the potential to be reversed, if we act quickly enough!

Predicting Patterns of Defaunation

If we are to halt or even slow the current mass extinction, we need to identify both the causes of defaunation and the traits that make certain species so vulnerable to human disruption. The main drivers of defaunation are overexploitation of species, habitat destruction and introduced invasive species. These threats have all increased in severity over the past decade and look set to continue. In addition to these long-term threats, climate change is rapidly becoming the biggest threat to biodiversity. Most threatened species are under pressure from multiple human threats, but our understanding of the complex interactions and feedback loops between different threats is still in it’s infancy. It’s clear though that these threats do not act in isolation; a species trying to track suitable habitat as it moves with climate change will find that task much harder if habitat loss and fragmentation is also occurring.

Researchers have highlighted a number of life history and biological traits that tend to make species more vulnerable to human impacts. For example, species that have a small geographic range, large body size and produce just a few offspring after a long-development process, are more likely to be threatened with extinction due to human activities. However, our understanding of the traits that influence species’ extinction risk doesn’t help conservation as much as you might expect, because the relationship between these traits and extinction risk is often idiosyncratic and highly context-dependent. These relationships may also be more variable and weaker for individual populations than for whole species, making population declines more difficult to predict than whole-species extinctions. Defaunation, ultimately, is a synergistic function of the traits a species possess and the nature of the threat(s) it is exposed to.

Disrupting Ecosystems and Communities

The loss of biodiversity through defaunation is not just a concern because of the aesthetic appeal of an individual species, or of a world rich in diversity in general. It is also a major concern because defaunation will likely have a negative impact on the ecosystem goods and services upon which we rely upon for our wellbeing and survival. In fact, biodiversity loss is thought to be comparable to other threats such as pollution in terms of it’s impact on ecosystem function. Defaunation can be expected to have a negative impact on our food, water and health, as well as our psychological wellbeing.

Food

Insect pollination is required for the continued production of 75% of the World’s crops, and is responsible for 10% of the economic value of the entire World’s food supply. Declines in pollinators are now a major problem, particularly in Northern Europe and the USA, and have been linked to declines in insect-pollinated plants. Biodiversity, particularly of small vertebrates, is provides crucial pest control services, valued at around $4.5 billion a year in the USA alone. Declines in small vertebrate populations are linked to cascading changes in the whole ecosystem which allow increases in pest abundance and, consequently, a loss of plant biomass. If the plant in question is a crop or food source, the results can be catastrophic.

Nurtient Cycling and Decomposition

Invertebrates are also very important for their roles in decomposition and nutrient cycling. Defaunation can reduce these important services, and cause changes in the patterns of nutrient cycling that can have knock-on effects on a huge variety of ecosystems. Likewise, large vertebrates that roam large home ranges are important in connecting ecosystems and transferring energy between them, and yet these species are often the most severely impacted by human activities.

Water

Another key ecosystem service is the provision of clean, fresh water. Research has shown that declines in amphibian populations can result in increases in algae, reduced nitrogen uptake and changes to oxygen availability in the water. This too will likely have major knock-on effects for other species (including ourselves!).

Health and Medicine

Finally, we can expect defaunation to negatively affect our health. Species that are more robust to human disturbance are often also better at carrying and transmitting zoonotic diseases (diseases that are carried by animals and transferred to humans), and altering ecosystem dynamics can change behaviours that influence transmission rates. Defaunation is likely to also reduce the availability of pharmaceutical compounds and alter the dynamics of disease regulation. All of this may mean that defaunation leads to an increase disease and a reduction in the availability of therapeutic compounds.

The impact of defaunation is less about the absolute loss of biodiversity and more about the local shifts in species composition and functional groups, which alter ecosystem function and ultimately, our food, water and health. However, reductions in species exploitation and land-use change are two feasible actions that can be achieved rapidly and may buy us enough time to address other drivers of defaunation such as climate change. Globally, we need to reduce and more evenly distribute our consumption if we are to change current trends in defaunation, and open the possibility for refaunation.

Original Article:

() Science

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This research was made possible by funding from the Natural Environment Research Council (NERC), the National Council for Scientific and Technological Development (CNPQ), the Foundation for the Development of UNESP, the Sao Paolo Research Foundation, the Joint Nature Conservation Committee (JNCC), the National Science Foundation (NSF) and the National Autonomous University of Mexico/a>.

Evolving Endemism in East Africa’s Sky Islands

By Claire Asher, on 8 August 2014

The World’s biodiversity is not evenly distributed. Some regions are hot spots for species richness, and biologists have been trying better to understand why these regions are special and what drives evolution and diversification. A recent paper by GEE’s Dr Julia Day and recent PhD graduate Dr Siobhan Cox, investigated the diversification of White-Eye Birds in East Africa’s Afromontane Biodiversity hotspot. Their results indicate that speciation in these birds has likely been driven by adaptation to a gradient of environmental conditions.

The East Afromontane Biodiversity Hotspot (EABH) is one of the most biodiverse regions on Earth, but it is under constant threat from increasing urbanisation in the area, which is predicted to continue over coming decades. It is therefore crucial to quantify what biodiversity is found in this hotspot, and understand the evolutionary processes that have made it a hotspot. The geography in this region is quite special, and is thought to have been a key factor driving high levels of species richness here. The Afromontane region is formed of a chain of ancient massifs (mountains created by faults and flexures in the Earth’s crust) and relatively young volcanoes. The low-lying regions between these peaks are covered in arid savannah, but montane forests appear on the peaks above about 800m. These forests exists as “ecological islands”, isolated from each other since the early Oligocene around 33 million years ago. Before this, conditions in the region were less arid and continuous forests covered the mountains and the valleys. As the forests retracted and fragmented, their inhabitants became isolated from one another, and this may have led to the emergence of new species, unique to each isolated montane fragment.

A Brief Introduction to Speciation
The processes by which new species arise depend upon the circumstances. Traditionally, speciation was thought to occur as a result of geographic separation of populations of a single ‘parent’ species. Once isolated and unable to interbreed, the two populations would slowly diverge from each other both due to random genetic change and adaptation to differing conditions. If enough time passed before the two populations came into contact with each other again, then they would eventually be so distinct that they were unable to interbreed even if they were reunited, and therefore should be classified as separate species. This is the standard model of speciation, known as allopatric speciation. It is now appreciated that new species can arise even without geographical isolation in a process known as sympatric speciation, often this can be caused by isolation of other kinds, such as behavioural isolation or through selective mate choice. It is generally accepted, however, that speciation requires, at least, a massive reduction in the rates of interbreeding between two populations or subspecies. Interbreeding will tend to restrain divergence as it mixes genes between the populations.

Evolving Endemism
There are two main hypotheses for how the extraordinarily high levels of endemism arose on the montane forest ‘islands’:

  1. The Montane Speciation Model suggests that montane ‘islands’ became refugia for species as they tracked suitable conditions up the mountain. This idea is based on a general theory for speciation and divergence known as ‘niche conservatism’, which suggests that geographical isolation of populations is driven by an inability to adapt to changing conditions. Once isolated, populations begin to diverge from one-another and over time this generates very high species richness.
  2. The Gradient Speciation Model by contrast, hypotheses that new species emerge as a result of adaptation to different conditions along a gradient. In this model, adaptation and niche divergence drive speciation, and we expect to find related species living in adjacent habitats.

The EABH is home to over 1300 described species of bird, of which 110 are known to exist nowhere else on Earth. In a recent paper in Molecular Ecology, Dr Day, along with colleagues at the Natural History Museum (Tring, Hertfordshire), the Technical University of Munich and the National Museums of Kenya, investigated the pattern of divergence in African montane white-eyes (Zosterops), a group of small, gregarious birds. Each montane forest fragment houses a single, endemic species, while other species live on real islands, and others live in other habitats on the mainland. This makes them an ideal group to test the competing hypotheses of niche conservatism and niche divergence.

The authors collected mitochondrial and genomic DNA samples for 148 birds from 15 species found across the EABH and elsewhere. They estimated the evolutionary timing of each species’ divergence based on both geological and molecular data, to investigate whether the montane taxa speciated in their current habitat or elsewhere, and whether they speciated before or after the climatic changes that isolated forest fragments.

A Late Pleistocene Colonisation
Based on molecular data, the authors estimate that White-eyes colonised Africa in the late Pleistocene, around 1.55 million years ago, and then exhibited brief pulses of diversification from 0.9 million years ago until around 0.3 million years ago. The genus Zosterops therefore colonised the region long after the montane forest habitat had fragmented into ecological islands, discounting the montane speciation hypothesis. Montane species diverged from their lowland sisters around 1 million years ago, during the last major wet phase. In some cases, montane species were found to be older than species found in neighbouring lowland areas, indicating colonisation in the other direction. They found no evidence that diversification of the White-eyes corresponded with volcanic activity in the region, which has previously been suggested.

They found that many of the so-called ‘species’ of Zosterops in fact include multiple sub-species, and they found strong support for already identified subspecies. This suggests that different species and subspecies independently colonised the montane habitat, and have remained more or less the same since. That the lowland savannahs that exist between the montane islands is a strong barrier that isolates montane populations is strongly supported by their results – species on neighbouring sky islands are very different from each other genetically, indicating they have not interbred for a great deal of evolutionary time. This is similar to the pattern of colonisation and diversification seen in White-eye species that live on real islands, which likely present similar evolutionary pressures to the ecological islands found in fragmented habitats.

Overall, their results support a niche divergence explanation of speciation in Montane White-Eyes, consistent with the gradient hypothesis, and ruling out niche conservatism models, such as the montane speciation hypothesis. However, the authors point out that their results do not distinguish between the gradient hypothesis and similar alternative, the vanishing refugia model, which suggests that speciation occurs through adaptation to less favourable habitats as suitable habitat contracts and refugia become unable to maintain viable populations. Further research is needed to conclusively distinguish between these models. The relative climatic stability of the highland montane habitats, couples with frequent climatic fluctuations in low-land areas may have played a key role in diversification in White-eyes, and may be a key driver of endemism in this region.

Original Article:

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This research was made possible by funding from the Natural Environment Research Council (NERC).

Predicting Extinction Risk:
The Importance of Life History and Demography

By Claire Asher, on 28 July 2014

The changing climate is no longer simply a concern for the future, it is a reality. Understanding how the biodiversity that we share our planet with will respond to climate change is a key step in developing long-term strategies to conserve it. Recent research by UCL CBER’s Dr Richard Pearson identifies the key characteristics that are likely to influence extinction risk due to climate change, and shows that existing conservation indicators such as the IUCN red list may contain the data necessary to make these predictions.

Human activities have been negatively impacting biodiversity for centuries, and conservationists have developed a number of different indicator lists which attempt to classify species’ extinction risk. However, these lists were created to measure human impacts such as as habitat loss, hunting and introduction of invasive species. These impacts will continue to be a major issue for biodiversity, but may be dwarfed in the future as climate change takes hold. Can the indices and data we already have be used to predict extinction risk from climate change? Or does climate change represent a new type of threat, needing new indices?

Studies have previously identified the ecological and biological traits that are characteristic of threatened or declining species. However, it is not clear how well these traits predict the future risk of climate-induced extinction. In February this year, GEE’s Dr Richard Pearson, in collaboration with colleagues at the American Museum of Natural History, Stony Brook University and the University of Adelaide, published a paper in Nature which attempted to address these questions. Most studies that have considered the impact of climate change on species’ extinctions have attempted to predict changes in the distribution of suitable habitats and measure extinction risk in terms of whether the species is likely to be able to find habitat to live in. However, such studies rarely consider how a species’ traits such as life history and spatial characteristics will influence their ability to persist through changes in climate. In this study, Pearson and colleagues coupled ecological niche models with demographic models, and developed a generic life history method to estimate extinction risk over the coming century.

Modelling Extinction
The authors then tested their models on ecological and spatial traits for 36 reptile and amphibian species in the USA. Using commonly available life history variables, they found that their models could accurately predict extinction risk between 2000 and 2010. They then utilised the same traits and models to predict future extinction risk under two climate models – a high emissions scenario and a policy scenario aimed at curbing emissions. Average extinction risk for the 36 species studied was 28% under the high emissions scenario, dropping to 23% under strict policy intervention. This seems like a very small difference for a significant intervention – it’s important to note that the same estimates indicated an average extinction risk of just 1% in the absence of any climate change at all.

One of the most important determinants of extinction risk in reptiles and amphibians was occupied area, which represents the range of climatic and habitat conditions the species can survive in. Species with a larger occupied area tended to be more robust to climate change, presumably because they are already adapted to a wider range of habitats and climates. Other key variables influencing extinction risk include population size and generation length. In many cases, traits interacted to determine species risk, for example extinction risk was strongly influenced by interactions between occupied area and generation length. Including many different traits can therefore greatly improve the accuracy of predictions. Recent trends tended to be less informative than spatial, demographic and life history traits, particularly under the high emissions scenario, suggesting that the impacts of climate change we have observed so far are likely to become less and less relevant as climate change accelerates.

The majority of variables that showed a significant impact on extinction risk are already included in major conservation assessments and indices, meaning that data and monitoring programs already in place may be better at predicting extinction risk under climate change than we might have expected. Climate change may not be fundamentally different from other human threats such as habitat loss and hunting, at least in terms of our ability to assess extinction risk. Conservation initiatives should focus on species who currently occupy a small and declining area and have a small population size. Regardless of the policy future, conservation actions will need to consider and account for climate change if they are to prove effective.

Original Article:

() Life History and Spatial Traits Predict Extinction Risk Due to Climate Change Nature

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This research was made possible by funding from the National Aeronautics and Space Administration (NASA) and the Australian Research Council

It Pays to Be Different:
Evolutionary Distinctiveness and Conservation Priorities

By Claire Asher, on 15 July 2014

The world is currently experiencing an extinction crisis. A mass extinction on a scale not seen since the dinosaurs. While conservationists work tirelessly to try and protect the World’s biodiversity, it will not be possible to save everything, and it is important to focus conservation efforts intelligently. Evolutionary distinctiveness is a measure of how isolated a species is on it’s family tree – how long ago it split off from its nearest living relative. A recent paper co-authored by UCL GEE’s Dr David Redding, published in Current Biology, assessed how effective evolutionary distinctiveness is a tool for identifying bird species of conservation priority. Current conservation efforts are missing some of the most evolutionarily distinct species.

Evolutionary distinctiveness (ED) is measured as the distance along the evolutionary tree from one species to it’s nearest relative. It can be used as a measure of how much evolutionary ‘information’ would be lost if this species were to become extinct. We have good estimates of these distances for birds as we have been able to put dates on the evolutionary tree based on fossil records and molecular data. A recent analysis of nearly 10,000 known bird species, by researchers at Yale University, Imperial College London, University of Sheffield, Simon Fraser University, University of Tasmania and University College London, showed some patterns we might have expected, for example, evolutionary distinctiveness is highest in isolated regions (e.g. Australia, New Zealand and Madagascar) and regions with higher species richness tended to have more evolutionary distinct birds. However, there were also some unexpected results. For example, ED wasn’t strongly related to latitude, a pattern predicted by the idea that the tropics act as a ‘museum’ for ancient lineages, nor was ED related to a species’ range-size, which has previously been predicted theoretically.

Evolutionary distinctiveness showed little relationship with conservation status – some of the most threatened distinct species are found outside of biodiverse regions that are usually the target of conservation efforts. This means that, when we consider only species richness or total biodiversity to identify regions to conserve, we may be missing a great deal of evolutionary information. Instead, basing areas of conservation priority on the evolutionary distinctiveness of their flora and fauna may offer a more efficient and effective way to maximise the evolutionary variation we keep.

The paper also released the first formal list of ‘EDGE birds’ – EDGE stands for “Evolutionary Distinctive and Globally Endangered” and is a metric combining ED with the IUCN Red List. The list includes the Giant Ibis, the New Caledonian Owlet-Nightjar, the California Condor, the Kakapo, the Philippine Eagle, the Christmas Island Frigatebird and the Kagu, all of which are listed as either Critically Endangered or Endangered.

The most evolutionary distinct birds include both common species and rare species, both isolated and wildly distributed species, and are found in almost every environment on Earth. Current conservation efforts that focus on tropical regions with high species richness may be neglecting many evolutionary distinct species, whose extinction would represent the loss of a great deal of ‘evolutionary information’. Evolutionary distinctiveness could offer a powerful tool to supplement current criteria for identifying conservation priorities.

Original Article:

() Current Biology

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This research was made possible by funding from the Natural Environment Research Council (NERC), the Natural Sciences and Engineering Research Council (NSERC), the National Science Foundation, and the National Aeronautics and Space Administration (NASA)

Synthetic Biology and Conservation

By Claire Asher, on 7 July 2014

Synthetic biology, a hybrid between Engineering and Biology, is an emerging field of research promising to change the way we think about manufacturing, medicine, food production, and even conservation and sustainability. Oryx front cover
A review paper released this month in Oryx, authored by Dr Kent Redford, Professor William Adams, Dr Rob Carlson, Bertina Ceccarelli and CBER’s Professor Georgina Mace, discusses the possibilities and consequences of synthetic biology for biodiversity conservation. Synthetic biology aims to engineer the natural world to generate novel parts and systems that can be used to tackle real world problems such as genetic disease, food security, invasive species and climate change. It’s implications are far reaching, and although research in synthetic biology began decades ago, conservation biologists have only recently begun to take notice and appreciate it’s relevance to the conservation of biological diversity. A conference organised by the Wildlife Conservation Society in 2013 discussed the relationship between synthetic biology and conservation, and included speakers from both fields.

Finding Common Ground
It might be surprising to find that, despite a similar background in biological research, the shared knowledge and language of conservationists and synthetic biologists is relatively limited. Further, many synthetic biologists come from an engineering background, with little training in ecology. This can make communication between scientists in these fields more difficult, and may have slowed the pace at which synthetic biology has interfaced with conservation science. The two disciplines also employ different methods and think about nature in different ways. Synthetic biology is largely conducted within large, highly controlled laboratory conditions, whilst ecologists work on complex, interrelated natural systems with a major social and political component. Conservationists, working in a high-stakes field and learning from past mistakes, tend to be quite risk-averse in their practice of conservation, whilst synthetic biologists, working in a new science with much to gain from experimentation, tend to be more in favour of taking large risks. They may also have different outlooks on the future of biodiversity – conservations tend to be more pessimistic about the future, mourning past biodiversity loss, whilst synthetic biologists have an upbeat attitude, envisaging the applications of exciting research. Despite these (extremely generalised) differences, the conference revealed interest and excitement on both sides about the possibility of collaborating, and a mutual appreciation that the major challenges of the Anthropocene are human influences on climate, biodiversity and ecosystems. Finding practical, long-lasting and safe solutions to the plethora of challenges currently facing humanity, is of mutual interest.

Mitigating Risks and Maximising Benefits
The possible applications of synthetic biology to conservation are many. Synthetic biology might enable us to develop more efficient methods of energy production, freeing up habitat to recover. It could mitigate the effects of greenhouse gas emissions by releasing carbon-consuming algae. It could revive extinct species such as mammoths and dodos in a process known as ‘de-extinction’. It could engineer coral that is tolerant to increases in ocean temperature and acidity, conditions which are predicted to worsen under climate change. It could help to control or eradicate invasive species. It could restore degraded land and water for agriculture, sparing the need to destroy more natural habitat. It could even create pesticide- and parasite-resistant bees that can continue to pollinate our crops generations into the future.

However, he potential risks of synthetic biology to conservation are as many as the potential benefits. The effects of synthetic biology on conservation could be direct, (e.g. engineering resistant species), or they could be indirect (e.g. changes in land use). These effects could be negative, for example, if they lead to land use change of primary habitat as has been associated with GMOs and biofuels. They could also be positive, for example if they reduce the impact of human activities, allowing habitat to recover to its natural state. Synthetic biology might lead to unexpected impacts on ecosystem dynamics and risks the unintended escape of novel organisms into open ecosystems. Releasing synthetically engineered organisms into wild environments could alter ecosystems, reduce natural genetic variability or lead to hybridisation events that might display native flora and fauna, and generate new invasive species. Synthetic biology might also distract attention and funds from more traditional conservation efforts, whilst attracting protest from human rights and environmental organisations. Both conservationists and synthetic biologists are conscious of these potential risks, and are committed to careful consideration on a case-by-case basis. Not all synthetic biology is the same; some could be of huge potential benefit to conservation and sustainability whilst carrying minimal risks, and it is these that we should pursue.

Original Article:

() Oryx

Measure Twice, Cut Once:
Quantifying Biases in Sexual Selection Studies

By Claire Asher, on 25 June 2014

Bateman’s principles are conceptually quite simple, but form the basis of our understanding of sexual selection across the animal kingdom. First proposed in 1948, Bateman’s three principles posit that sexual selection is more intense in males than in females for three reasons:

1) males show more variability in the number of mates they have (mating success);
2) males show more variability in the number of offspring they have (reproductive success);
3) the slope of the relationship between mating and reproductive success is steeper in males;

Together, this summarises our basic view of sexual selection in the majority of sexually reproducing species – males that do well, do very well and we expect more intense sexual selection because of it.

Biased Traditions
Traditionally, most studies investigating these relationships have measured mating success by counting the number of females a male produces offspring with. This method is biased though, as it assumes that every mating results in offspring, which is unlikely to be true. Further, it assumes that every fertilisation produces an offspring, which ignores cases where embryos die before birth. Using offspring counts as a way to measure mating success might not be accurate but it is certainly more practical – behavioural observations of actual mating would be very time consuming and nearly impossible for some species. However, until now no study has attempted to quantify the importance of these biases in calculating and testing Bateman’s principles.

Carefully Observed
To address this issue, GEE researchers Dr Julie Collet and Dr Rebecca Dean, in collaboration with researchers at the University of Oxford, University of Queensland, Uppsala University and the University of East Anglia, investigated mating and reproductive success in Red Junglefowl (Gallus gallus). They recorded matings and collected all eggs laid from 13 groupings of 3 males and 4 females (mimicking natural conditions). They began by using classic techniques to estimate Bateman’s gradients – they inferred mating success from the number of females they sired an offspring with. They found twice as much variability in male mating success, and four times as much variance in male reproductive success (the actual number of offspring a male produced) compared with females. Mating success and reproductive success were strongly related – differences between individuals in mating success explained 57% of variance in reproductive success in males, but only 24% in females, and the slope of the relationship was steeper in males.

A Male Red Jungle Fowl

They then repeated their analysis but with a more accurate measure of mating success – the actual number of partners and matings observed. In this study, 30% of pairs that mated did not produce any offspring together and would be ignored by the traditional measure of ‘mating success’. Including these matings reduced the variability in mating success in both males and females. It also reduced the explanatory power of mating success – using this technique they found that variation in mating success actually explained 43% of variation in male reproductive success, and just 5% of variation in female reproductive success. This suggests that traditional methods for measuring Bateman’s principles are likely to be overestimating their importance and the extent of sexual selection on males.

Covarying Factors
Reproductive success is not just a product of how many mates you have. The fecundity of your mate is also a crucial factor, and in species where females mate with multiple males, your share of her offspring is also a key variable. The authors investigated whether these variables tend to be related and whether multivariate analyses that take them all into account better explain the overall reproductive success of a male. Their multivariate model explained the variance in male mating success better than the standard approach and found that mating success, paternity share and mate fecundity together are responsible for the variance in male reproductive success. The authors estimate that by ignoring these other factors, other studies may overestimate the Bateman gradient by as much as 150%!

This study shows the importance of investigating the biases we introduce into our science. These biases may sometimes be inevitable, if excluding them is extremely time consuming or difficult. But we must try to understand the influence of these biases in order to draw informed conclusions from our data. Here, GEE researchers demonstrate how using biased measures of mating success can cause scientists to overestimate the opportunity for sexual selection on males. This effect is likely to be largest for species which have small clutch sizes and in which sperm competition plays a key role. Where possible, studies investigating sexual selection should include accurate measures of mating success, and include other variables such as paternity share and mate fecundity in a multivariate approach in order to best understand Bateman’s principles and the relationship between mating and reproductive success in both sexes.

Original Article:

() Proceedings of the Royal Society B

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This research was made possible by funding from the Natural Environment Research Council (NERC), the Biotechnology and Biological Sciences Research Council (BBSRC) and Marie Curie Action.

Technology for Nature?

By Claire Asher, on 16 June 2014

Many of our greatest technological advances have tended to mark disaster for nature. Cars guzzle fossil fuels and contribute to global warming; industrialised farming practices cause habitat loss and pollution; computers and mobile phones require harmful mining procedures to harvest rare metals. But increasingly, ecologists and conservation biologists are asking whether we can use technology to help nature. On 10th June 2014, UCL’s Center for Biodiversity and Environment Research (CBER) hosted academics from the National Museum of Natural History, Paris, the Zoological Society of London and the Natural History Museum, London for a workshop on “Technology for Nature”. The workshop formed part of a series of public debates and workshops organised in collaboration with the French Embassy, around the theme of the ‘State of Nature’.

Technology for Nature Workshop

The workshop discussed some of the latest technologies available to monitor biodiversity and how these might be harnessed in combination with citizen science to better understand the natural world around us. Citizen science, which engages members of the public in collecting and processing data about nature, is a powerful tool enabling scientists to collect much larger quantities of data on populations of key species. Citizen science projects not only provide biologists with vastly more data than they could ever hope to collect on their own, but it also serves to engage members of the public with the natural world, and raise awareness of key environmental issues.

Following the workshop, UCL also hosted an evening debate in collaboration with colleagues at the French Embassy, London. Professor Romain Julliard from the National Museum of Natural History, Paris, and Professor Kate Jones from UCL’s CBER discussed how new technologies can be used to understand and predict the impact of humans on the natural world, and whether these technologies can be used to inspire and engage the public with the environment around them.

Technology for Nature Debate

Professor Julliard is the Scientific Director of Vigie Nature, a project to monitor trends in various widespread species including butterflies, birds, bees and flowers, using citizen scientists in France. Professor Jones holds the chair of Ecology and Biodiversity at UCL and the Zoological Society of London, and has been involved in a number of projects utilising citizen scientists to monitor populations of bats both in the UK and across Europe. She started the iBats project, which uses volunteers to collect acoustic recordings of bat calls which a computer algorithm can then use to identify the species, and has used citizen science to process data from this project through Bat Detective.

The meeting last week brought together academics from a range of different institutions with a shared interest in monitoring biodiversity to better understand how humans are impacting upon it. We hope this will lead to new projects and collaborations to monitor biodiversity and gain vital data that is needed to assess and ultimately mitigate our impact on the animals and plants we share the planet with.

Nice Flies Don’t Finish Last:
Meiotic Drive and Sexual Selection in Stalk-Eyed Flies

By Claire Asher, on 12 June 2014

While it might seem as though our genes are all working together for our own good, some of them are actually rather selfish. Scientists have known about ‘selfish genetic elements’ for nearly a century, but research to understand their behaviour and effects is ongoing. Recent research in GEE reveals how sexually selected traits are signalling selfish genetic elements (or a lack of them) in the same way they are used to signal male quality and health.

Selfish Genes and the Balance of the Sexes
Selfish genetic elements are variants (alleles) of genes which, rather than acting to the benefit of the individual, act in their own interest to ensure maximum replication of themselves. One type of selfishness that genes can exhibit is called meiotic drive, and is associated with alterations to the sex ratio of offspring. Sex ratios for most species tend towards 1:1, for sound evolutionary reasons, but this isn’t in the best interest of all genes. Genes that lie on one of the sex chromosomes (X or Y in mammals, Z or W in birds) are not equally successful in both sexes – if you happen to lie on the X chromosome, for example, there’ll be two copies of you in each female offspring but only a single copy in male offspring. Meiotic drive occurs when selfish genetic elements skew the sex ratio in order to favour their own replication – usually caused by genes on the X chromosome creating a female-biased sex ratio.

Sex ratios tend to be roughly even in nature because offspring sex ratio is a trait that is under strong stabilising selection. In populations with a biased sex ratio, the underrepresented sex immediately becomes extremely valuable, simply by virtue of its rarity. Imagine a village consisting of 20 women and a single man – that man would undoubtedly have the pick of the ladies, and would likely produce more offspring. If you are the mother of that male, you’ll have done very well for yourself. In a population with a skewed sex ratio, offspring of the underrepresented sex are more valuable, and natural selection to produce them is very powerful. Any mechanism by which females could identify a male that will produce these valuable offspring would be strongly favoured by selection.

Photograph of a male stalk-eyed fly.

A Male Stalk-Eyed Fly (Teleopsis dalmanni)

Meiotic Drive
Stalk-eyed flies are found in Africa and Southeast Asia and show striking sexual dimorphism (physical differences between the sexes). Both males and females have their eyes placed on the end of long stalk-like appendages, but in males these ‘stalks’ can be very long. This is a sexually selected trait – males with longer eyestalks are healthier, carry fewer harmful mutations and are better at attracting females, meaning they tend to have more offspring.

In the laboratory, stalk-eyed flies often produce very female-biased broods; this is thought to be a result of meiotic drive that causes male sperm (carrying a Y chromosome) to degenerate, but female sperm (carrying an X chromosome) to persist. Researchers believe that the length of eyestalks may be linked to meiotic drive, and long-eye stalks may signal to females that a male does not carry the harmful selfish allele. In the laboratory, it has already been shown that males selectively bred for short-eye spans tend to produce female-biased broods, and four loci on the X-chromosome have been identified that are associated with female-bias.

Beyond the Laboratory – Tests in Wild Populations
Expanding on this research, academics in GEE wanted to investigate this phenomenon in the wild. Their work, recently published in Heredity, investigated eyespan and sex ratio biases in 12 populations of wild stalk-eyed flies in Malaysia. Dr Alison Cotton and colleagues at UCL and the University of Debrecen, Hungary, collected nearly 500 wild stalk-eyed flies, measured their eyestalks and other physical characteristics, and collected DNA samples. The researchers used a technique known as microsatellite genotyping to identify regions of the X-chromosome where genes responsible for meiotic drive and for eyestalk length were located. Microsatellites are repeating DNA sequences that tend to vary in their length (the number of repeats) between individuals. Microsatellites can be used as genomic markers for nearby genes of interest – we expect that different microsatellite alleles will be consistently associated with different alleles of interesting genes nearby. Because they vary in physical length, microsatellite alleles can easily be identified by separating DNA sequences out according to size.

The authors found that one microsatellite, ms395, was strongly associated with male eyestalk length. This relationship was not found in females. Longer ms395 alleles tended to be associated with smaller male eyespans.

Photograph of Stalk-eyed flies, (Teleopsis dalmanni)

Stalk-eyed flies, (Teleopsis dalmanni)

Males collected from 5 wild populations were taken back to the lab where they were allowed to mate, so that researchers could investigate the sex ratio of their offspring. Around a quarter of wild-caught males produced biased sex ratios, most often producing more females than males. Males producing sex-biased offspring tended to have smaller eyestalks, when their overall body size was controlled for. They also tended to have longer ms395 alleles.

The authors were able to show that microsatellite ms395 is associated both with sex ratio biases and with male eyestalk length, suggesting that the genes controlling eyestalk length and meiotic drive are located on the X-chromosome near ms395, and that eyespan may be a signal of the genetic quality of the male. For females, a male that carries a selfish genetic element that causes meiotic drive (and a lack of male offspring) is of poor genetic quality, but by preferentially mating with males with longer eyestalks, females can avoid these harmful genes. This may indicate that eyestalks are an example of the good genes hypothesis for sexual selection, which suggests that physical characteristics involved in mate choice are associated with alleles that produce high quality males and are therefore used as an honest signal of the quality of potential mates.

This study is the first to demonstrate meiotic drive in wild populations of the stalk-eyed fly (Teleopsis dalmanni) and adds strong support to previous research suggesting that male eyestalk length is a signal of the presence of meiotic drive. As long as these genes remain in close proximity to each other through evolutionary time, the association should be maintained and eyestalks can be used as a reliable way for females to identify good quality males. Or at least males that are likely to give them a nice even sex ratio in their offspring.

Original Article:

() Heredity

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This research was made possible by funding from the Natural Environment Research Council (NERC), the Engineering and Physical Sciences Research Council (EPSRC) and Marie Curie Action.

Finding a Place to Call Home:
Translocation and the Plight of the Hihi

By Claire Asher, on 16 May 2014

Climate change alters how climate is distributed both geographically and temporally. Over the coming decades, for species sensitive to climatic variables, it may become a case of ‘relocate or die’ – those species that are not able to shift their populations from old, unsuitable habitat into newly emerging suitable habitat, in line with climate change, will likely go extinct. Conservationists can provide a helping hand to species in this position, however – translocation programs aim to establish populations in appropriate habitat when the species is unlikely to reach it on their own. Determining whether translocations are likely to be necessary in the future, what populations to move and where to move them are complex questions to answer, however. Recent work by researchers at the Institute of Zoology (part of the Center for Ecology and Evolution and affiliated with UCL’s GEE department) developed a framework for understanding species’ relationships with climate and identifying potential translocation sites which will provide suitable habitat through future climate change. For one of New Zealand’s endemic birds, the Hihi, translocation to sites further south may be it’s best chance of long-term survival.

Hihi, endangered bird endemic to New Zealand

The climate is changing. Changes in temperature, rainfall and seasonality are occurring globally, and we are already measuring the effects on wildlife. Often, conditions are shifting geographically, and many species will find that their current range no longer overlaps with any suitable habitat (human land-use change isn’t helping!). In these cases, some species will be able to shift their ranges to account for this, but many species will be unable to do change quickly enough to keep up and instead face extinction. Humans can intervene here by moving endangered species to more suitable habitat, but translocation is expensive and it is crucial to select the new location carefully if the population is to have a chance of succeeding. IoZ researchers set out to develop a statistical framework for determining suitable translocation habitat, using one of New Zealands most endearing but endangered endemics, the Hihi (Notiomystis cincta), to test the framework.

The population of Hihis in Tiritiri Mantangi island offers a special opportunity to study the direct effects of climate change without other variables such as food ability confounding the results. This is because they have been provided supplementary food for nearly two decades. Using data on the reproductive success of females in this population, combined with climate data, Dr Aliénor Chauvenet and Dr Nathalie Pettorelli from the Institute of Zoology, along with colleagues at Imperial College London and Massey University in New Zealand, were able to show that Hihi populations are effected by the climate even when food availability is removed from the equation.

Next, using mathematical modelling, the authors tried to predict the future of Hihi populations, using different simulated changes in climate based upon the variables that were found to be most important in influencing current Hihi populations on Tiritiri Mantangi. Changes in temperature, as well as increases in climate variability had a significant influence on the survival of simulated Hihi populations. The final step was to again use mathematical modelling to predict and map suitable Hihi habitat both now, and in the future. Again, this modelling showed that current Hihi populations are most strongly influenced by temperature, a key variable in determining habitat suitability, with rainfall as another important influence.

Looking forward, under models of predicted future climate change, suitable Hihi habitat is expected to move south. The north of New Zealand, which currently offers highly suitable habitat, is predicted to become almost entirely unsuitable over the next few decades. The most successful reintroduced population of Hihis, as well as the largest and last remaining natural Hihi population both stand to lose suitable habitat by 2050. New suitable habitat is expected to emerge in the southern end of the North Island, as well as the northern part of the South Island, where historically conditions have not been suitable for Hihis.

Because Hihis show population declines as temperatures warm even when we control for food availability, even careful management of existing population may prove ineffective under future climate change. Instead, translocation may provide the only solution to guarantee the long-term survival of the Hihi in New Zealand. Although translocations traditionally perform the role of reintroduction – returning a species to part of it’s historical range – future plans for endangered species like the Hihi need to take climate change into consideration. We should opt for ‘assisted colonisation’ – introducing populations to new habitat that is likely to persist (and perhaps even become more suitable) through future climate change. In this way we can attempt to ‘future-proof’ our conservation efforts and hopefully ensure the survival of many species which might otherwise go extinct as the climate changes.

Original Article:

() Journal of Applied Ecology

This research was made possible by funding from AXA Research and Research Councils UK .