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It Pays to Be Different:
Evolutionary Distinctiveness and Conservation Priorities

ClaireAsher15 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

nerc-logo-115nsf1nserc_logo_eNasa-logo

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)

Two’s Company, Three’s a crowd:
The Evolution of Two Sexes

ClaireAsher6 May 2014

You’ve probably never given much consideration to why there are men and women. Or, more specifically, why there are two sexes, rather than one, three or 50. But this is a question that has been keeping some scientists awake at night for decades. Recent research in the department of Genetics, Evolution and Environment used mathematical models of evolution to investigate how the evolution of the two sexes was influenced by the inheritance patterns of the energy-producing organelle, mitochondria. The results of this model contradict previous work supporting the idea that inheritance of mitochondria through only one parent might explain the emergence of two sexes. The evolutionary dynamics of mitochondrial inheritance are more complex than previously thought.

Sexual reproduction is a beneficial thing, in evolutionary terms, but this benefit doesn’t depend upon there being different sexes, only on there being two individuals sharing their genes to produce an offspring. This system would also work with no sexes at all (everyone can mate with everyone), or with many sexes. In fact, two is actually the worst number you could have picked – with two sexes any individual is limited to an available pool of mates just 50% of the population. With three sexes, this pool would increase to 66% of the population, with four 75%, and so on. So why have most sexually-reproducing species on settled on two sexes?

In a few previous GEE blog articles (see here and here), I have discussed the phenomenon known as ‘uniparental mitochondrial inheritance’ (UPI), in which mitochondria, organelles found in our cells that are responsible for generating energy, are inherited only through the maternal line – that is, you inherit all of your mitochondria from your mother and none from your father. UPI is found in many living things, although some species do things a bit differently and there are many different ways to achieve the same result. Work by GEE researcher Professor John Allen has previously shown that the mitochondria within egg cells in jellyfish, fruit flies and fish are largely inactive; this inactivity allows for a perfect ‘mitochondrial template’ to be passed on to the offspring and prevent the accumulation of mutations through the generations. Essentially, this is why aging isn’t heritable. It wouldn’t work to inactivate sperm mitochondria because they need so much energy for all that swimming, so if we did inherit mitochondria from our fathers they would probably be mutated. UPI is also thought to help evolution remove harmful mutations from the population and reduce conflict and promote coadpatation between the mitochondrial symbiont and its host cell.

Fertilisation So, UPI makes a lot of sense, evolutionarily, and some scientists think it might also explain why we have two sexes, as opposed to any other mating system. It’s important to be clear, when we talk about having two sexes we’re saying nothing about the external differences between the sexes (sexual dimorphism) observed in many multicellular organisms. We’re talking about the existence of two ‘mating types’, such that individuals cannot mate with members of the same type. Recent research by another group of GEE academics including Professor Andrew Pomiankowski, Dr Nick Lane and Professor Robert Seymour, investigated the evolution of UPI and in particular it’s relationship with the evolution of a two-sex mating system. We might expect a strong link between UPI and the existence of two sexes, since uniparental inheritance immediately generates differences between the two mating partners, and ensures that reproduction is not possible unless one member of each ‘type’ is present. Although UPI is often thought to have been a key driver in the evolution of mating types, there have been few investigations of what conditions are needed for the fitness benefits of UPI to actively drive the emergence of two mating types. So the authors developed a new mathematical model of mitochondrial inheritance and the evolution of UPI in a population where biparental inheritance (BPI) is the norm. They incorporated mitochondrial mutation (which might sometimes be selfish) and selection into the model, and included different mating types.

The model agreed with a great deal of previous work that indicates that UPI tends to increase fitness. It does so slowly, with selection acting cumulatively across many generations to remove less fit mitochondrial variants and increase fitness for UPI individuals. In a population of individuals where mitochondria is inherited biparentally, a new mutation causing UPI exists in a single individual. Slowly UPI improves the fitness of cells by reducing the number of mutated mitochondria they carry, and the UPI mutation might start to spread in the population. The problem is, as it spreads the benefits of UPI are inevitably leaked into the rest of the BPI population – UPI individuals mate with BPI individuals producing some BPI offspring who carry the fitter mitochondria from their UPI parent. This leaking of benefits means that the fitness benefits of UPI are frequency-dependent; the more common UPI becomes in a population, the less each UPI individual benefits from the reproductive strategy. This makes it hard for UPI to fully take over a population – their model tended instead to produce mixed populations with some UPI and some BPI individuals interbreeding.

Mitochondrial Evolution - Leaking of beneficial mutatations

Leaking of fit mitochondrial (blue) into BPI cells (a)

If the researchers included mating types in the model at the start of it’s evolutionary run, then UPI could become associated with specific mating types and in this situation, so long as mutation rates were high or each cell carried many mitochondria, UPI could spread to fixation in the population. But UPI itself was not able to alter the number or existence of mating types. The authors suggest that this may explain the continuum of UPI levels we observe in nature. For any given species, the occurrence of UPI will depend upon the evolutionary starting point, energetic demands, mutation rates and the selfish (or unselfish) nature of mutations.

Although most people never even consider why we have two sexes, male and female, the evolution of a two mating-type system is seemingly paradoxical and many theories and hypotheses have been proposed to explain it. One such explanation is that uniparental inheritance, which is critical for stabilising the mitochondria-cell symbiosis and preventing the accumulation of harmful mutations, may have driven the evolution of two sexes. However, mathematical modelling by scientists in GEE suggests this is not the case, and UPI more likely evolved after the two mating-type system emerged. In their model, although UPI initially spreads through populations, it’s fitness benefits are frequency-dependent, meaning it only rarely takes over an entire population. Populations in which all members inherit mitochondrial uniparentally are only possible when a mutation causing UPI becomes tighly linked to genes that determine mating type. The initial emergence of two mating types still requires an explanation independent from mitochondrial inheritance patterns.

Original Article:

() Proceedings of the Royal Society B: Biological Sciences

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

Dating Mammalian Evolution

ClaireAsher28 March 2014

When the age of the dinosaurs ended around 65 million years ago, mammals stepped in to fill the gap, and the age of the placentals began. However, whether early placental mammals were already present on Earth before the demise of the dinosaurs has been the subject of a long standing debate. Recent research in GEE used genomic data, in combination with fossil evidence, to show that the earliest placental mammals were indeed scurrying between the feet of dinosaurs.

Shrew-like mammals scurry between the feet of dinosaursThe huge diversity of placental mammals on Earth today first appeared shortly after the mass extinction event that killed the dinosaurs. It is thought that the loss of the dinosaurs, along with much of life on Earth, freed up niches which placental mammals to evolved to fill. But were early placental mammals present, waiting in the wings, during the age of the dinosaurs, or did they appear rapidly after their demise? One recent study suggested that, based on fossil evidence, the placental mammals must have appeared after the cretaceous-tertiary boundary (KT) when dinosaurs and most life on Earth was wiped out. However, a recent paper by GEE’s Mario dos Reis and Ziheng Yang, in collaboration with Philip Donoghue from the University of Bristol, highlights flaws in the methods used in this study, and utilitsed a more thorough approach to show that early placental mammals likely predated the KT boundary.

Using genetic sequence data from over 14,000 genes, combined with fossil evidence, GEE researchers applied 3 alternative statistical methods to estimate the age of the earliest placental mammal; ancestor to all modern placental mammals. Although different statistical methods yielded slightly different estimates, and differed in their accuracy, they all agreed that placental mammals must have already been around before the dinosaurs went extinct. The adaptive radiation of mammals that occurred after the extinction of the dinosaurs was dramatic, but it was initiated by a few shrew-like species which had already evolved. This study highlights the importance of using statistical methods to estimate the true age of ancestral species; the age of the oldest fossils is not the same as the age of the ancestral species that gave rise to them, and statistical techniques must be employed to estimate this. Using both molecular and fossil evidence to inform estimates also provides more robust evidence for the true age of the first placental mammals, and the theory that the earliest ancestors of placentals predated the disappearance of the dinosaurs.

Original Article:

This research was made possible by funding from the Biotechnology and Biological Sciences Research Council (BBSRC).

It’s All in the Wrist

ClaireAsher20 December 2013

The evolution of the primate wrist has been dramatic, enabling primates to adapt to a wide variety of lifestyles and walking styles, including tree-swinging, climbing and terrestrial walking both on four legs and two. In hominids, the evolution of the bipedal gait freed up the forelimbs for tool use, and the wrist evolved independently from the feet enabling increasing dexterity that was crucial to human evolution. Recent research in GEE has provided a more thorough analysis of primate wrist evolution, and shed light on a long-standing debate in human evolution: did humans evolve from tree-swingers or knuckle-walkers?

Primates use their limbs to move in a wide variety of different ways, many of which are not seen in other animals alive today, such as vertical clinging, swinging and leaping, and upright walking. Furthermore, within primates, some species have moved towards a more upright stance, freeing the forelimbs for other tasks. This is thought to have been a key aspect of human evolution, increasing our ability to develop and use complex tools, and possibly even playing a role in the evolution of gesture and language. The morphological evolution of primate wrist bones has therefore been of great interest to evolutionary biologists.

Comparative studies looking at humans and other living and extinct apes and monkeys have previously attempted to deduce the early evolution of the human skeleton, in particular how our bipedal stance evolved. However, many of these studies have attempted to determine the rate of evolution (the speed of ticking of the evolutionary clock) using morphological characteristics, which may not provide an accurate view. Recent research by GEE academics, in collaboration with the University of Kent and the Max Planck Institute, has attempted a more rigorous analysis of primate wrist-bone evolution by mapping morphological features onto an independently-generated phylogenetic tree, using molecular methods to estimate the speed of evolution. This method allowed the authors to detect multiple independent appearances of the same feature, as well as more accurately measuring the speed of wrist evolution.

Gorilla Wrist Bones Dr Kivell (University of Kent) and UCL’s Anna Barros and Dr Smaers, compared wrist bone features across 24 living primate species and 16 extinct species. Primate wrists are composed of between 8 and 9 separate bones, and they discovered differing evolutionary patterns for different bones, indicating that each bone evolves at least partly independently from the others. Some of the evolutionary changes that occurred during primate evolution are shared between species which move in similar ways, whilst others are shared between closely related species, regardless of locomotion. Hominids tended to show more morphological variation than monkeys, suggesting stronger selection on the hominid wrist, possible relating to rapid and major changes in body size and locomotion in these species.

This study also sheds light on a long-standing debate over the early evolution of bipedalism in hominids; competing hypotheses have suggested that humans evolved to an upright position from a knuckle-walking stance (e.g. modern Gorillas), or that they evolved from an aboreal, tree-swinging ancestor. The results of this study show adaptations in the hominid wrist bone, which appeared in parallel with Gorillas and Chimpanzees, that are consistent with increased weight being placed on the wrist during knuckle-walking. Thus, it seems more likely that humans evolved from a knuckle-walking, terrestrial ancestor.

Our bipedal stance came with a huge number of skeletal adaptations, and enabled us to adapt to new environments. It may also have been crucial in freeing up our hands for other tasks, which in turn played a role in our intellectual development. Understanding how our skeleton, particularly our hands and feet, evolved through the primate lineage therefore sheds light on some of the deepest aspects of humanity. The bones in the primate wrist have evolved at least partly independently from each other, and this has generated a large variety of wrist morphologies, adapting different primate species to different modes of locomotion. Early hominids likely evolved their bipedal stance from a knuckle-walking ancestor, rather than an arboreal tree-swinger.

Original Article:

() BMC Evolutionary Biology



This research was made possible by funding from the Natural Environment Research Council (NERC), the Natural Sciences and Engineering Research Council of Canada (NSERC), the Fundação para a Ciência e a Tecnologia , the Max Planck Society , and a General Motors Women in Science and Mathematics Award

Size Matters: Why Reduced Sexual Ornaments are Rarely Seen

ClaireAsher29 October 2013

Across the animal kingdom, males have evolved fancy physical ornaments, songs and courtship rituals, all in an attempt to attract the opposite sex. Most of the male ornaments and sexually-selected traits biologists tend to study are large, elaborate and flamboyant. But mathematical models predict that sexual selection is just as likely to make an ornament smaller or more modest as it is to make it more elaborate. Recent research by Dr Sam Tazzyman and Prof Andrew Pomiankowski from UCL’s Department of Genetics, Evolution and Environment, in collaboration with Prof Yoh Iwasa at Kyushu University, investigates why male ornaments tend to get bigger rather than smaller.

Male and Female Red Deer
Image by Deepsky, Creative Commons Licence

Sexual selection is the process whereby traits are favoured because they increase an individual’s success at obtaining mates, often at the expense of survival or condition. Sexual selection is a special case of natural selection, where natural selection is concerned with increasing the overall fitness of an organism. Sexual selection may act in opposition to natural selection, when traits that make you more attractive to the opposite sex also make you less fit in other ways. In these cases, the form a trait takes may be somewhere between the most attractive (sexual selection optimum) and the most fit (natural selection optimum). Sexual selection has been the focus of a great deal of evolutionary research, both experimental and theoretical, because it has the power to generate extreme physical and behavioural adaptations: huge antlers, complicated courtship displays, brightly coloured plumage, etc. Most research has focussed on bright, bold, exaggerated traits like these. But theory suggests that sexual selection should be just as likely to drive traits to be less extreme (than the natural selection optimum) as it is to make them more extreme. So why don’t we see sexually reduced traits much in nature?

First, Tazzyman and collegues searched the literature on mate choice and sexual selection for examples of reduced sexual traits – that is, cases in which females prefer males with a trait smaller, duller or less elaborate than the natural selection optimum. They found that for many types of trait, reduction simply isn’t possible, or is extremely difficult to define. For example, when a sexually-selected trait is a particular colour of a patch of plumage, how can we define exaggeration or reduction in this trait? Is the size of the patch most relevant, or the hue or saturation of colour? Similarly, for many traits, the natural selection optimum might be zero – no trait at all. For example, in many species the male is brightly coloured while the female is dull, here the dull colouration can be considered no trait and is assumed to be the natural selection optimum. Likewise, in many species the males carry physical adornments such as the red crests (or combs) of many gamefowl, which are totally absent in females.

Male and Female Junglefowl

Certainly, these issues with definition occur most frequently for colour, pheromone and behavioural traits. Morphological traits tend to lend themselves more readily to being classified on a simple scale, in which both exaggeration and reduction of that trait is possible. There are a few cases of females showing a preference for a smaller trait, but these examples are few and far between. Of 40 sexual traits for which both elaboration and reduction could be defined, 34 were found to be subject to sexual selection for exaggeration.

This imbalance may be partly explained by our own observation bias – smaller traits may be more difficult to detect and so tend not to become the subject of study. But, it is unlikely this is the full explanation. However, it seems that females may suffer a similar problem; if biologists aren’t noticing small ornaments, maybe the females aren’t either. This is one of three possible hypotheses that Tazzyman and colleagues tested to explain the apparent asymmetry in the direction of sexual selection. Male ornaments are signals, aimed at attracting a female – if that trait cannot easily be seen or detected by the female, then it cannot serve it’s purpose. Consistent with this, a mathematical model of sexual selection assuming asymmetrical signalling efficacy (where smaller traits are less effective at conveying their message) showed that exaggerated traits were more likely to undergo the ‘runaway’ selection characteristic of sexually-selected ornaments.

Peacock and Peahen
Image by ToastyKen, CC Licence

Their models also ruled out two other possible explanations – that it is more costly for a female to prefer a small trait than a large one, and that is it more costly for a male to carry a small trait than a large one. Neither of these models resulted in a bias towards exaggeration. Only models including an asymmetry in the efficacy of signalling produced results that mirror what we observe in nature.

Sexual selection acts upon traits that make one sex more attractive to the other, and can favour characteristics that are otherwise detrimental to survival or condition. Sexual selection has the power to generate the bright, flamboyant, exaggerated characteristics such as antlers that we see in many animals. Although many theoretical models predict both exaggeration and reduction in sexual traits, in wild populations, we rarely see this – almost all documented sexual traits are more extreme than their natural selection optimum. Sexual traits act as signals to the opposite sex, and this may explain why in the wild, sexual selection tends to exaggerate and elaborate traits which are more visible to females and so more effective at communicating their message.

Original Article:

() Evolution

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

Maintaining the Status Quo:
Constraints on the Evolution of Gene Regulation

ClaireAsher10 September 2013

Every living cell, whether solitary or part of a larger multicellular organism, is an extremely complex system, involving a multitude of simultaneous chemical reactions regulated by proteins and RNA. Keeping this machine running relies upon a careful balance of gene expression and protein degradation, and cells must be prepared to modulate these processes in response to environmental variation (both internal and external). Homeostatic mechanisms can be an efficient way to regulate gene expression, however one key mechanism – negative autoregulation – is rarely used in organisms like flies and humans. Mathematical modelling by GEE’s Max Reuter and Andrew Pomiankowski shows that evolutionary constraints in the evolution of negative feedback may exist for species who carry multiple copies of each chromosome in their cells.


A Eukaryotic (Animal) Cell and a Prokaryotic (Bacterial) Cell

Homeostasis: From Radiators to Cells
One of the simplest ways to regulate any system is through negative feedback, whereby a particular process is inhibited by the products of that process. This is the system employed by central-heating systems, which use the temperature to regulate the action of a radiator. The radiator pumps out heat, and when the thermometer detects too much heat in the room, it signals the radiator to stop. Negative feedback systems can be highly efficient, stable and responsive.

Negative feedback, or homeostasis, would also be a sensible way to regulate the expression of genes within a cell – a particular gene would continue to be expressed and produce its protein product until there is enough of that product in the cell, at which point expression would stop. This system would be sensitive to the demands of the cell – if the product was being used up quickly, then expression would continue as long as demand was high. In fact, many simple, single-celled organisms, such as E. coli, use this system to respond quickly to changes in their environment.

Around half of all genes in Escherichia coli are regulated by this kind of negative feedback loop, known as negative autoregulation. However, when we look at other organisms such as yeast (Saccharoymyces cerevisiae), fruit flies (Drosophila melanogaster), and humans, we find a very different picture – almost no genes show signs of negative autoregulation (around 2%). If negative autoregulation is such a neat solution to apparently common problem, why aren’t humans and flies using it?

By Ehamberg (Own work)
[CC-BY-SA-3.0 or GFDL],
via Wikimedia Commons

A Matter of Ploidy
One of the key differences between humans and E. coli (although probably not the one that springs to mind!), is that E. coli carry only a single copy of each gene in each cell. They are haploid, with a single circular chromosome in each cell that carries a single copy of each gene in the E. coli genome. By contrast, humans, yeast and fruit flies are all diploid, meaning that they carry two copies of each gene in every cell. Our genes are split up into many, straight chromosomes, and we have two copies of each chromosome. Recent research in the department of GEE has used a mathematical modelling approach to investigate how diploidy (having two sets of chromosomes) might constrain the evolution of negative autoregulation.

In a paper in PLoS Computational Biology in March this year, Dr Alexander Stewart, Professor Rob Seymour, Professor Andrew Pomiankowski and Dr Max Reuter from UCL’s GEE produced a mathematical model of how gene regulation might evolve differently in species with one or two sets of chromosomes. Their model focuses on mutations in the promoters of genes, which alter how other protein molecules interact with and repress the expression of those genes.

In haploids, with a single copy of each gene, negative autoregulation produces very tight regulation of gene expression, giving a very rapid response to changing demand. Likewise, in a diploid species with two identical copies of a particular gene, negative autoregulation tends to be beneficial and achieves very efficient gene regulation.

Constraints in the Evolution of Regulation
The problem arises when the diploid carries two different variants of the same gene. This would be the situation whenever a new mutation arises – new mutations appear in a single copy of a particular gene. For a new mutation to be favoured and spread through the population, it must be able to do well, at least initially, as a single copy. The mutated gene must be able to work well alongside the original version. And this is where the problem arises. Stewart, Seymour, Pomiankowski and Reuter (2013) found that mutations that altered the negative autoregulation of a gene didn’t tend to play well with others. Their model considered mutations that alter the strength of the binding site – essentially how strongly regulated that gene is. An individual carrying one strongly regulated gene and one weakly regulated gene actually did worse than an individual with two weakly regulated genes. These heterozygote individuals responded more slowly to changes in demand, and there was more noise in the system. This situation, known as underdominance, where a genetic variant has a lower fitness in the heterozygote form, could be a major constraint to evolution.

under-dominance_crop

Underdominance in negatively autoregulated systems arises because of the disparity in binding site strength between the two different copies of a gene. As each gene pumps out gene product, the stronger binding site is quickly suppressed by the product produced by both genes. It takes much longer for the weaker binding site to be suppressed, as it requires more product to be activated, and most of this is being used up by the stronger binding site. Compared to a haploid, the strong site shows faster response times but the weak site shows a much slower response time, and this averages out to an overall slower response.

Stewart et al (2013)’s model showed that the extent of underdominance depended on how different the two genetic variants were. Large differences in the strength of their binding sites reduced response time and created more noise than smaller differences. Slower response times and increased noise in heterozygotes mean that the maximum strength of regulation achievable in a diploid may be as much as ten-fold lower than in haploids.

Because very small differences between genetic variants in their binding site strength did not experience such a strong effect of underdominance, they were more likely to lead to the evolution of autoregulation. Evolution in diploids could proceed through many very small changes, however there is also likely to be lower limit on the size of mutations – very small changes cannot be ‘seen’ by natural selection and are unlikely to spread. Likewise, multiple binding sites, each relatively weak but which act together cooperatively, were also more likely to overcome the issue of underdominance in the model. However, in general, diploids had a much harder time evolving negative feedback as a mechanism for gene regulation. This evolutionary constraint might have forced diploids such as fruit flies and humans to develop alternative mechanisms to achieve rapid responses, such as increased rates of protein degradation or alternative regulatory mechanisms.

Original Article:

() PLOS Biology

This research was made possible by funding from the Natural Environment Research Council (NERC), the Engineering and Physical Sciences Research Council (EPSRC), and the McDonnell Foundation

The Battle of the Sexes:
Sexually Antagonistic Genes in Small Populations

ClaireAsher18 July 2013

By definition, males and females are physically different. In some cases, these differences are restricted to the sex organs, but in many species males and females also differ in their physical appearance and behaviour. What makes you a good male does not necessarily make you a good female, and the benefit of some genes depends upon which sex they find themselves in. These antagonistic genes have sex-dependent fitness effects, and can be a source of genetic variation in natural populations. Research in GEE shows that in small populations, chance events can alter the frequency of antagonistic mutations, and alter the balance of fitness between the sexes. Small populations tend to produce either good males and poor females, or good females and poor males, but not both. This phenomenon could have interesting implications for dispersal and fitness, especially in fragmented populations.

Differences in physical appearance between the sexes is known as sexual dimorphism, and occurs because characteristics that make you good at being male are often different from the characteristics that make you good at being female. A brightly coloured male may get more females because he is more visible or attractive, but a brightly coloured female doesn’t lay more eggs, she just gets eaten.

Sexual dimorphism allows males and females to independently adapt to different optima. The problem is dimorphism is actually quite hard to achieve. Males and females of the same species share, more or less, the same genome. Some species, such as birds and mammals, have sex-specific genes and chromosomes (e.g. the Y chromosome), but these represent a very small proportion of their genes, and many species achieve sexual dimorphism without any sex chromosomes at all. For the most part, traits that differ between males and females are generated from the same set of genes. The evolution of dimorphic traits such as body size, plumage colour and antlers proceeds not through changes to gene function, but changes in gene expression.

Gene Expression and Sexual Dimorphism

Male and female Red Deer
(Cervus elaphus)

A gene that codes for a trait that is beneficial to males but detrimental to females can become sexually dimorphic if it is expressed only when it appears in males (or vice versa). This same gene, when it finds itself in a female body, simply isn’t expressed and does not exert its effect. So a female red deer carries the gene for antlers, but never grows any because the gene is silent.

Sex-specific gene expression is an elegant solution to the problem that males and females face different challenges in life. However, the road to sexual dimorphism is not that straight forward. For a new sexually dimorphic trait to evolve, it must first appear as a novel mutation in a pre-existing gene. At first, it will be expressed just like most other genes – equally in both males and females. This mutation might do great when it finds itself in a male, allowing him to produce more offspring, but when it appears in a female, it would be harmful, reducing the number of offspring produced. For this new mutation to be successful and spread through the population, it needs to avoid the negative fitness effects that come from being expressed in a female. At this stage, a second mutation altering gene regulation – so that the gene is expressed only in males – would be hugely beneficial, but this mutation may take time to arise by chance.

There are many examples in nature of sexually dimorphic traits – genetic variants expressed in one sex but not another. But scientists are increasingly finding mutations that haven’t made it to this happy equilibrium yet – their fitness effect is sex-dependent but they are still expressed in both males and females. These genes are known as ‘sexually antagonistic’ and are thought to be a major source of genetic variation within populations.

Generating Variability
Normally, a gene that has a detrimental effect (i.e. reduces how many offspring you produce) is quickly removed from the population by natural selection. Sexually antagonistic genes are different because their detrimental effect is only seen by natural selection when the mutation appears in one sex. Half the time, the mutation is beneficial, and half the time it is harmful. Overall, the effect of the gene can even out to be essentially neutral. Neutral mutations can stick around in a population for ages, although they may be lost, or spread, by chance.

Chance, also known as genetic drift, can change the frequency of mutations in a population irrespective of their fitness effects, and the effect of chance is much greater in smaller populations. Sexually antagonistic genes may be particularly susceptible to genetic drift because their effect is, on average, neutral. Most theoretical and empirical studies of sexual antagonism use very large populations with high genetic diversity, where the influence of genetic drift is very small. Researchers in GEE have been investigating the evolution of sexual antagonism in small populations to see how chance might influence their frequency.

The fruit fly,
Drosophila melanogaster

The Role of Chance
In a recent paper in Evolution, Jack Hesketh, Kevin Fowler and Max Reuter from GEE looked at how small populations of the fruit fly Drosophila melanogaster evolved, and how sex-specific fitness changed under the influence of genetic drift, through the random spread of sexually antagonistic genes. Four populations of 100 flies were maintained for 80 generations, and the fitness of both larvae and adults was measured in terms of survival (larvae), fertilisation success (males) and egg-laying (females).

Over 80 generations of evolution in the lab, the four fruit fly populations diverged in terms of fitness. Average fitness across the sexes didn’t differ significantly between populations, but there was a strong interaction between population and sex – some populations produced very fit females and unfit males whilst others produced fit males and unfit females. This effect was not present for larval fitness however, which makes sense since larvae are primarily concerned with growth and not reproduction. In the original source populations, some individuals carried mutations beneficial to females, whilst others carried mutations beneficial to males. In this experiment, through the process of genetic drift, different populations ended up with a different selection of these mutations – some populations kept hold of the genetic variants favourable to females and consequently produce very fit females but relatively crap males (and vice versa).

This study shows that in real populations, genetic drift may lead to population-divergence in sexually antagonistic genes. This could have interesting repercussions for fragmented populations where different fragments may diverge differently in terms of sexual antagonism. Dispersal in this situation could be extremely favourable – a fit male in a population full of fit males would be faced with stiff competition, but if he wandered over into a neighbouring population full of unfit males, he would presumably have his pick of the ladies. Max Reuter and colleagues in GEE hope to continue to investigate this phenomenon and its consequences in natural populations.

Original Article:

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

How Energy Shapes Life: Our Mitochondrial Partners

ClaireAsher21 June 2013

Every cell in our bodies is a collaborative effort. A collaboration that dates back to just after the dawn of life itself, and marks one of the deepest divides in the tree of life. This symbiosis has had remarkably far-reaching effects, and is now thought to be key to understanding sex, ageing and death. The symbiotic entity in question is the mitochondrion; the power house of the cell. Biologists are increasingly realising the centrality of energy in understanding life, and a special issue of Philosophical Transactions of the Royal Society, introduced by Nick Lane, focuses on the synthesis of energy, genes and evolution.

Mitonucleus in Blue
Artwork by Odra Noel www.odranoel.eu
Image Used with Permission

Around 1.5 billion years ago, a simple, single-celled bacterium engulfed another one. But it didn’t eat it. Instead, the two cells started working together, and over the following millennia developed a cooperative relationship that laid the foundation for multicellular life and for diversification on a scale never seen before. This symbiotic relationship founded a new type of life – the eukaryote. Unlike their prokaryote ancestors, the eukaryotes had a special advantage: they now had internal membranes. This enabled them to generate energy more efficiently, utilising a force generated across a membrane, known as the proton-motive force. This allowed them to support bigger cells, a wider variety of diets, and ultimately led some eukaryotes to group together into multicellular, sexual organisms such as plants and animals.

Hand Over Your Genes!
Since mitochondria originated as free-living single celled organisms, they came complete with their own genetic information. As the cooperative partnership between the eukaryote host and its mitochondrial partners developed, the majority of these genes were transferred to the nuclear (host cell) genome. Bizarrely, though, a few genes remained with the mitochondria. In fact, the same few genes stayed put in almost all eukaryotes, even though this process happened many times independently. So what is so special about these genes? Why keep them in the mitochondria when it is costly to do so?

A Mitochondrion

A Rapid Response System
It is thought these genes remain in the mitochondria because they are needed there to allow individual mitochondria to respond rapidly to changes in the energy demands of the cell. When mitochondria are out-of-sync with their surroundings, they start generating dangerous ‘reactive oxygen species’ (ROS), also known as free radicals. Free radicals are famous for causing cancer, and this is because they act as mutagens, causing changes to DNA they encounter. Mutations caused by ROS can cause all sorts of problems, not just cancer, and many of the diseases of old age are thought to be caused by ROS mutations.

So, we need to keep a small set of genes – those that code for key components of the respiratory chain that generates energy in mitochondria – in close proximity to their site of use so that they can quickly respond to the ever-changing cellular environment. This is also true for chloroplasts in plants, and recent research by Puthiyaveetil and colleagues in GEE lends support for this explanation. They have found evidence for a chemical partnership, unique to eukaryotes, which may be important in regulating chloroplast function to minimise ROS production.

Both mitochondria and chloroplasts have held onto a few genes in order to allow a rapid response to changes in demand. Trouble is, by keeping those genes there, they are vulnerable to attack from any free radicals that are generated. Mutations in these genes can often cause the production of more free radicals, causing a downward spiral that eventually leads to the death of the cell.

Unusual Inheritance

Fertilisation

Mitochondrial genes are not inherited in the same way as normal nuclear genes. The majority of our genes (residing in the nucleus) are inherited biparentally, that is, we inherit half from our mother and half from our father. Mitochondrial genes, on the other hand, are inherited only in the maternal line, through the egg. Mitochondria are also present in sperm cells – they have to be, since they are crucial for providing energy to power all that intense swimming – but sperm mitochondria are killed shortly after fertilisation. Recent research by John Allen in GEE suggests that uniparental inheritance of mitochondrial genes relates back to those pesky free radicals.

In sperm cells, mitochondria are working overtime to make sure the sperm has the energy to swim and find the egg. In the process they are churning out free radicals, and damaging the mitochondrial DNA. The mitochondria inside sperm start to suffer from the ravages of old age. But we don’t want to pass on old mitochondria to our offspring. It seems evolution has found an elegant solution – switch off the mitochondria in egg cells and pass these young mitochondria on to your offspring. De Paula and colleagues looked at the mitochondria in eggs, sperm and the bell of moon jellyfish (Aurelia aurita) and found egg mitochondria were largely inactive and simple in structure. Egg mitochondria also showed reduced levels of gene expression, an almost non-existent membrane potential and produced no free radicals, indicating that they were not actively generating energy. Eggs don’t need that much energy compared to sperm, and they can borrow what they do need from other cells. By switching off the mitochondria in eggs, and making sure these are the only ones passed on to the next generation, eukaryotes can reduce the build-up of harmful age-related mutations in mitochondria from generation to generation.

The Moon Jellyfish (Aurelia aurita)

Energy, Mitochondria and the Meaning of Life
The generation of energy is central to life. Mitochondria generate energy in all eukaryotic cells (animals, plants, fungi), and the symbiotic event that brought them into the eukaryotic cell changed life on Earth forever. Mitochondria proved massively beneficial, allowing eukaryotes to try new things, and ultimately produce the huge diversity of multicellular life we see today. However, housing another genome inside the cell came with nuances of its own, which led us to have sex, to age and die. Recent research in GEE highlights one way in which evolution has overcome one of these nuances – by switching off mitochondria in egg cells, offspring can inherit an undamaged copy, and because of this, ageing is not heritable. Other research in plants is broadening our understanding of why these genes are stored inside the mitochondria and chloroplasts in the first place. Throughout a plethora of different disciplines, mitochondria are proving crucial to understanding the fundamentals of life.

Original Articles:

() Philosophical Transactions of the Royal Society B

() Philosophical Transactions of the Royal Society B

Introduction to the Special Issue:

() Philosophical Transactions of the Royal Society B

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

Continental Catfish Show No Sign of Stopping

ClaireAsher14 June 2013

The tree of life is a vast tangle of branches and twigs representing around 9 million species. Understanding the patterns and processes by which these species originated is a fundamental topic in evolutionary biology. Previous studies have suggested that the generation of new species may not be uniform over time, often with an initial burst of speciation, slowing as the lineage expands to fill the available niches. However, recent research in the department of GEE suggests this may not always be the case, and a previous focus on island species may have skewed our perspective of species accumulation.

When a new lineage begins to diverge, adapting to exploit new habitats or lifestyles, this often leads to an adaptive radiation, with many new species appearing over a short space of time. This initial rush of new species eventually begins to slow, as all the available niches become saturated, and slowly speciation grinds to a halt. This is the traditional view of how lineages have diversified to produce the vast array of species we see today (as well as many who have long since gone extinct). However, much of the research in this area has focussed on species confined to islands and lakes, where different processes may influence the appearance of new species. Continental species have a larger area to expand into, and a wider array of climatic conditions to cope with, providing a different set of parameters which may influence speciation. Recent research in the department of Genetics, Evolution and Environment suggests the pattern of species generation in continental lineages may differ from that of islands.

Tree of Life image © 2007 Tree of Life Web Project. Image of rose © 1999 Nick Kurzenko. Image of annelid worm © 2001 Greg W. Rouse

In their recent paper in Systematic Biology, Day and colleagues determined species relationships for 81 species of squeaker catfish from Africa in order to investigate the patterns of species generation and diversification during their 35 million year evolution. Using genetic data along with fossil evidence, they constructed a squeaker catfish tree and estimated divergence dates and historical geographic distributions. This tree revealed an almost constant rate of species generation over time. Across 35 million years of evolution, through major climatic and environmental changes, the squeaker catfish have been churning out new species at approximately 1 every 8 million years, and look set to keep going for another 90 million years, or so.

Syndontis 'squeaker' catfish. Photograph by Roger Bills

Syndontis ‘squeaker’ catfish . Photograph by

So why don’t the continental, river-dwelling catfish follow the same rules developed through years of studying island and lake-dwelling species? Continents are, of course, generally much larger than islands, and rivers provide more opportunity for movement than lakes. Continents allow for more constant species generation, as there is more space and habitat diversity available for species to move into and exploit. The climatic changes in Africa over the last 30 million years may have also helped the catfish maintain constant production of new species – creating a variable environment which is much less likely to become saturated with species. The squeaker catfish have survived through major tectonic activity in the East African Rift valley, including volcanoes and earthquakes, as well as huge climatic changes that influenced sea level and temperature. By combining phylogenetic and biogeographical data, Day et al suggest these environmental variations may have played an important role in African catfish diversification.

The processes shaping species diversification are varied and complex, and differ markedly between geographically isolated lineages (island / lake ecosystems) and wider ranging ones (e.g. continental rivers). Continental groups may take longer to reach species saturation, with environmental fluctuations facilitating continued species generation at a relatively constant rate. Moving beyond ‘model organisms’ and well-studied systems has the potential to reveal new processes and patterns, and illuminate old ones.

Original Article:

() Systematic Biology

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

Skulls and Teeth: Constraints on Mammalian Evolution

ClaireAsher7 June 2013

When we think about evolution, we tend to imagine the appearance and behaviour of animals as infinitely malleable, changing and adapting to perfectly suit the whim of natural selection. However, in many cases, evolution is actually surprisingly constrained. The potential for a species to evolve into new environments, diets or lifestyles may be limited if the necessary variation isn’t available in the population. In this case, the raw materials for natural selection to act upon are missing and a species cannot evolve in a particular direction. Evolutionary constraints may be developmental or genetic in origin, and may in part explain why some groups of species are more diverse than others.

Early in mammalian evolution, around 160 million years ago, mammals diverged into two main groups; placental mammals (e.g. humans, rats, elephants) and marsupials (e.g. kangaroos, possums, koalas). Placental and marsupial mammals use a different strategy for early development; mammalian infants develop either internally (placental mammals) or in a pouch (marsupials). Despite a similar period of evolutionary history, there are far fewer species of marsupials, and as a group they show less diversity in terms of locomotion and diet. New research suggests their unusual developmental strategy may have constrained their evolution, limiting the variety of present-day marsupials.

A Koala (Phascolarctos cinereus)
A Marsupial Mammal

Chipmunk

A Chipmunk (Neotamias umbrinus)
A Placental Mammal

Pouch-Living Limits Marsupial Diversity
Placental mammals give birth to reasonably well-developed young after a lengthy pregnancy. However, marsupials, such as kangaroos and koalas, do things a bit differently. The infant is ejected very early in development, and must crawl to a specialised pouch where it can complete the rest of its development, feeding by suckling. This developmental strategy is pretty demanding on the young marsupial, and requires that they are strong enough to crawl and suckle at a very young age. There is evidence that the shoulder has been constrained by the demands of crawling at a young age. Has suckling imposed similar constraints on the skull?

During development, embryonic connective tissue begins to form into bone through a process known as ossification. In marsupials, ossification in the skull and particularly in facial bones occurs much earlier in development compared to placental mammals. This pattern is probably necessary to allow marsupial young to suckle at such a young age. Early facial ossification has wide-ranging effects on brain, tooth and muscle development, and may have limited the diversity of facial shapes available to marsupials. Suckling may have been a major constraint on marsupial evolution.

Facial bones (viscerocranium)
and braincase (neurocranium)

In a recent study conducted in GEE, Bennett and Goswami (2013) measured a number of skull characteristics for 125 species of placental and marsupial mammals. Previous studies have failed to find evidence for evolutionary constraints affecting mammalian skulls, but these studies primarily focused on carnivores, and considered the whole skull at once. By looking at different regions of the skull separately, Bennett and Goswami found that marsupials exhibit less variation between species in the facial bones (viscerocranium) than placental mammals. This pattern is not present for the braincase (neurocranium), which is not involved in suckling behaviour, and where bones ossify much later. These results suggest that early suckling might have constrained the diversity of marsupial skull shapes, and may go some way to explaining why marsupials are less diverse.

Something to Get Your Teeth Into
Mammalian diversity has probably been constrained by a variety of factors, not just bone ossification. Another recent study from GEE and Earth Sciences by Halliday and Goswami (2013) showed that tooth growth patterns may have restricted the relative size and shape of mammalian teeth, potentially influencing diet. Mammalian tooth development is thought to proceed by an ‘inhibitory cascade’, whereby the growth of each developing tooth is controlled by a balance between stimulatory signals from the embryonic tissue, and inhibitory signals from the adjacent tooth. This results in the middle molar being intermediate in size between the first and last molar.

Coloured teeth

Lower right jaw of two early mammals, showing the first molar (yellow), second molar (green) and third molar (red).
Pentacodon occultus (left) – a very early insectivorous mammal
Hyracotherium (right) – the first horse, a browsing herbivore
Photograph by Thomas Halliday

Across 154 species of mammal, despite considerable variation in tooth shape and size, the relative sizes of the three molars conformed to the same basic pattern in about two thirds of species. The largest tooth was almost always either the first or last molar, in line with a common pattern of tooth development across all mammals. Diet is strongly related to tooth size and shape: mammals with a larger third molar (coloured red) tend to eat more plant matter, while mammals with a larger first molar (coloured yellow) tend to be meat-eaters. Across 180 million years of evolution, almost all mammals still conform to the same basic pattern of tooth development that their early ancestors used.

The Exception to the Rule
One extinct group of mammals, called condylarths, bucked the trend in molar shape. Their middle molar was largest, inconsistent with an inhibitory cascade. Perhaps this was an archaic adaptation to a new diet – condylarths were among the first omnivorous mammals, and a similar pattern is found in modern-day bears. The developmental constraint of the may not have been too strong for this particular deviation, though, and could have been achieved by a fairly simple modification to the inhibitory cascade.

Adaptation is not infinitely plastic. Natural selection can only work with the raw materials of variation in the population. Sometimes, one aspect of life constrains another, but if the pay-off is great enough, evolution will often find a way, despite the constraints.

Original Articles:

()Testing the Inhibitory Cascade Model in Mesozoic and Cenozoic Mammaliaforms BMC Evolutionary Biology 13: 79

 

This project was made possible by funding from the Natural Environment Research Council (NERC), as well as Abbey Research and Collaboration Awards and the University of London Central Research fund.