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

Claire Asher25 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


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.

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

Claire Asher12 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


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.

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

Claire Asher6 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.

Size Matters for Single-Celled Dating

Claire Asher24 April 2014

Size matters. Particularly when it comes to finding a mate. Across the animal kingdom, body size plays a crucial role in determining how successful individuals are at surviving and reproducing. Large males are often better at fighting off competing males, while large females generally produce more offspring. However, being big isn’t always best. In some environments, small individuals may have a better chance of survival. Choosing a partner the right size may help to ensure a good start in life for your offspring. Recent research in GEE suggests that even simple organisms such as yeast are able to choose the best size mate to ensure their offspring survive and reproduce.

In single-celled organisms, just like their multicellular counterparts, the ideal body size depends on surrounding conditions in the environment. In nutrient rich environments, larger cells do better, whilst in nutrient poor environments, smaller cells prevail. In many multi-cellular animals, females have been shown to select mates based on body size to ensure their offspring the best possible chances of survival. Are unicellular organisms also able to make these kinds of selections? A recent paper by GEE Researchers Dr Carl Smith, Prof. Andrew Pomiankowski and Dr Duncan Greig investigated this phenomenon in yeast.

The Curious Life-Cycle of Yeast
Yeast Life CycleYeast, being single-celled, are able to reproduce asexually – budding off a new copy of themselves. However, when times are hard, yeast can also enter a sexual phase of reproduction. When nutrient levels are low, a yeast cell will divide into sexual spores. These spores are haploid, carrying only one copy of each chromosome (rather than the usual two), making them analogous to sperm and egg cells. Spores will remain dormant until they sense an improvement in the environment, at which point they spring into action and try to find a mate. Spores come in two mating types and must always mate with another spore of the opposite type – a system based on mating pheromones released by spores to attract the opposite sex.

Body size is important in both the asexual and sexual phases of yeast reproduction. Yeast cells must reach a certain critical size before they can bud asexual copies of themselves, although this critical size is smaller in poorer environments. Likewise, during sexual reproduction, the cell size of the offspring is determined by the cell size of the two spores that fuse together. GEE researchers first investigated how body size influenced reproductive success in both phases of yeast reproduction. Cell size was an important influence on how quickly spores awoke from dormancy to begin searching for a sexual partner; large spores became active 38% more quickly in a nutrient-rich environment, whereas smaller spores were 63% faster when conditions were poor. Asexual reproduction was similarly affected, with large spores budding off asexual copies sooner in good environments and small spores budding sooner in bad environments. Size matters when it comes to yeast reproduction, but bigger isn’t always better.

Are Sexual Yeast Cells Selecting the Right Sized Partner for their Environment?
To answer this question, GEE Researchers created a mating-choice experiment, in which a haploid yeast cell of one mating type is presented with two cells of the opposite type, one small and one large. To mate, two of these haploid cells will fuse to form a single, diploid cell which can resume asexual reproduction. These experiments were performed with different sizes of focal yeast cell, and in different environments, to see whether the focal cells were able to select the best partner – one that would give the final fused cell the best chance of survival. This is a critical choice – mating in these single-celled organisms is an irreversible decision, the size of the ‘offspring’ cell is directly determined by the size of the two haploid cells that fuse, and cell size will influence how quickly the ‘offspring’ can reproduce.


The results of the experiment indicate that yeast cells are indeed able to make careful calculations about their choice of partner and select the one closest to the optimum size for the environment. In nutrient rich environments, yeast cells tended to select larger mates, whereas in poorer environments they tended to select smaller mates. This was true regardless of their own body size, indicating that cells were not simply mating with similar sized partners, but making a choice based upon the mates available and the environment around them. The authors suggest that such seemingly complex behaviour could be generated quite simply – if cells that are better adapted to their environment begin emitting these pheromones earlier, or produce them in larger amounts, they would be more easily detected by a prospective mate.

Size is a crucial determinant of success, survival and reproduction for most living organisms. However, the optimum size often depends upon environmental conditions, as GEE researchers have shown to be the case for yeast. For most organisms, selecting a mate is an important decision that will influence the success of their offspring. For yeast even more so, this decision is critical, as it is irreversible. A new paper from GEE researchers shows that yeast cells also consider the quality of their partner when mating. During sexual reproduction, yeast cells are able to select a mate of the optimum size for the environment, thereby improving the chances that the resulting offspring cell will reproduce.

Original Article:

() Ecology and Evolution

This research was made possible by funding from the Natural Environment Research Council (NERC), the Biotechnology and Biological Sciences Research Council (BBSRC), the Engineering and Physical Sciences Research Council (EPSRC), The Royal Society and the Max Planck Society.

Dating Mammalian Evolution

Claire Asher28 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).

The Delicate Balance of Effect and Response

Claire Asher18 February 2014

We may not always be aware of it, but many wild plants, animals, fungi and even bacteria, provide crucial services to us which keep the ecosystems of Earth functioning. Environmental changes caused by human activities are now threatening many species, and those that cannot withstand these changes may be lost forever, potentially taking the services they provide away. New research from GEE and collaborators worldwide aims to improve our understanding of how the traits and evolutionary histories of species influence their ability to provide essential ecosystem services, and to persist in the face of ongoing environmental change.

The diverse array of species we share planet Earth with, and the complex ecosystems they form, are crucial to our continued survival and well being. Species and ecosystems provide a huge number of ‘ecosystem services’ – functions such as nutrient cycling, waste decomposition, pollination and food, to name just a few, which humans rely on. However, many species are now under threat from human activities like deforestation, hunting and pollution. Scientists are working to understand how species and ecosystems will respond to our continued activities in the future, and particularly how this may effect the vital ecosystem services upon which we rely. Recent research by GEE’s Prof. Georgina Mace, in collaboration with researchers from Cordoba National Univerity, Imperial College London, VU University, Yale University and CSIC, has attempted to develop a new framework for risk assessing the effect of human activities on ecosystem services.

The framework considers two key aspects of species: their effect on the generation of a specific ecosystem service (e.g. seed dispersal), and their response to specific environmental pressures (e.g. drought). Both the effect of a species and the response of a species are underpinned by its traits, and each is influenced not by a single trait but a combination of traits. The response of a species will determine it’s ability to survive and flourish through future environmental changes and to continue to provide it’s ecosystem effects. However, only a species’ response is the subject of natural selection, via changes to the underlying traits; the effect of a species is merely a biproduct of traits selected for their influence on survival. In this way, the aspects of a species’ biology upon which we rely are only indirectly influenced by natural selection, and will only be maintained if the traits that generate them are beneficial through the environmental changes we cause. The framework developed by GEE researchers and collaborators considers how the response of species to envinmental stressors interacts with the effect of that species on key ecosystem services, and whether species with a large effect are more or less vulnerable to environmental change.

A third key factor influencing the sensitivity of ecosystem system services is the evolutionary relationships between species providing them. Closely related species often share similar traits, which may or may not result in them having similar effects and responses. If this is the case, then ecosystems in which a particular service is provided by a group of closely related species may be more vulnerable to environmental change, since those species may well share similar responses, and be sensitive to similar environmental pressures. Although many species’ traits are known to be similar amongst related species, because effects and responses are each the result of a combination of traits, it is not known whether this relationship is also common for these variables.

The new framework developed by GEE’s Professor Georgina Mace and collaborators attempts to address this by incorporating evolutionary relationships (phylogeny) into their response-effect model, and applying this model to 5 case studies. The case studies cover 5 species assemblages including a total of 480 species in Europe, Central America and Africa, for which response and effects could be estimated based on past studies of species’ traits and vulnerabilities. The case studies tended to show a strong relationship between phylogeny and both species’ effects on ecosystem services and their responses to environmental stressors. This indeed suggests that ecosystem services that rely upon closely related groups of species may be most at risk from environmental change. Cases where effects and responses are negatively correlated, so that the most influential species in terms of a given ecosystem service are also the most vulnerable to environmental stress, are most vulnerable to loss of that ecosystem service through human activities. Whether this type of relationship is common in nature remains to be investigated by future studies, and this framework provides a powerful basis with which to do so.

Our relentless demands on the natural world are inevitably leading to new pressures and stresses on natural populations, and it is of great concern that these pressures may negatively impact on the vital ecosystem services that we rely upon, often without even realising it. Ecosystem services provide us with food and fresh water, decompose our waste, recycle nutrients and remove harmful toxins. Without them our continued survival and well being would be seriously compromised. Scientists are still working to understand how species’ traits influence their ability to provide ecosystem services and their resilience to ongoing environmmental change. A new framework developed in collaboration between universities in the UK, Spain, Argentina, the USA and the Netherlands is beginning to shed light on the interaction between species’ traits, their effect on ecosystem services and their response to environmental change, and how these factors are influenced by evolutionary relationships between species. This framework offers a powerful new view of how the traits of species within an ecosystem translate into the ecosystem services upon which we are so reliant, and future research building upon this framework promises to improve our understanding of ecosystem services and environmental change.

Original Article:

() Ecology and Evolution

This research was made possible by funding from the Natural Environment Research Council (NERC), the Leverhulme Trust, and the US National Science Foundation

It’s All in the Wrist

Claire Asher20 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

The Transcriptional Profile of A ‘Wingman’

Claire Asher27 November 2013

In many species, males have special adaptations to attract females. From antlers to stalk-eyes, to bright plumage and beards, males across the animal kingdom work hard to look attractive to the opposite sex. In some species, looking good isn’t enough, though. Male wild turkeys need a less attractive ‘wingman’ to help him attract a woman. Wingman turkeys show less extreme sexual traits than the dominant males, and researchers from GEE have exploited this ‘intermediate phenotype’ to investigate how gene expression controls sexual traits. Subordinate male turkeys are physically demasculinised, and this is reflected in their gene expression. Whilst clearly male, these turkeys tend to express ‘male’ genes less and ‘female’ genes more, indicating that sexual phenotypes, at least in this species, exist upon a continuum. This has important implications for how we view sexual selection and sexual traits across the animal kingdom, as well as in our own species.

You might think this is a face only a mother could love, but to a female turkey, this guy is very attractive. Male wild turkeys have a number of physical traits that make them very, very sexy…. to female turkeys, at least. They are larger than females, their feathers are iridescent, their faces are bright red and adorned with caruncles, wattle and a snood. As they grow up, young male turkeys argue with their brothers for dominance. One brother wins, and the others become subordinate. These subordinate males rarely get the chance to mate themselves, but helping out their brother means passing on their genes indirectly. If, later in life, the dominant brother dies, the subordinate may get his chance in the limelight and develop a dominant phenotype. This shows just how plastic sex can be in the animal kingdom.

Differences in Gene Expression
Differences between the sexes form ‘sexual phenotypes’ that are largely the result of the differential expression of genes that are present in both sexes. Although sex chromosomes are also important in controlling the development of sexual traits, many genes on other chromosomes also contribute. Many genes show differences in expression between the sexes.

Theory suggests that genes expressed differently in different sexes are responsible for generating the sex-specific characteristics we observe. However, this hypothesis has been difficult to test in species where sex is binary. This is where wild turkeys come in handy – the existence of the subordinate male phenotype, with reduced sexual traits, provides a rare opportunity to decouple genetic sex and sex-biased gene expression. If sex-biased genes encode sex-specific phenotypes then the subordinate male phenotype should be expected to be the product of reduced expression of male-biased genes and increased expression of female-biased genes.

Researchers in GEE and the Department of Zoology, University of Oxford, investigated gene expression patterns in females, dominant and subordinate males. Around 2000 genes were male biased and nearly 3000 showed female bias.

Unravelling the ‘Wingman’ Phenotype
The gene expression patterns of subordinate males clearly clustered with dominant males. So subordinates are not intersex. However, there were subtle differences between the subordinate and dominant males. Subordinate males tended to express male-based genes at lower levels than dominant males, indicating transcriptional demasculinisation. They also expressed female-biased genes at a higher level than dominant males, suggesting transcriptional feminisation. Expressionally, subordinate males were less masculine and more feminine than dominant males. This is consistent with their visual appearance.

Furthermore, genes that were more strongly sex-based showed a greater level of demasculinisation in subordinates than those that were less strongly sex-biased. This suggests that the genes we find to be most strongly sex-biased may contribute the most to generating the male or female phenotype.

These patterns were also true for genes found on the z chromsome – the sex chromosome in birds (analogous to our ‘Y’ chromosome). However, the patterns were no stronger for these genes than for those on other chromosomes, suggesting that the sex chromosome does not contribute disproportionately to the male or female phenotype. This might come as a surprise – surely the sex chromosome should control sex? There is now a great deal of evidence that this isn’t the case, and many animals get on just fine without a sex chromosome at all!

Dominant and subordinate males reveal a continuum of sexual characteristics physically, and this is mirrored by gene expression patterns. Whilst clearly male, subordinate males showed up-regulated of ‘feminine’ genes and down-regulation of ‘masculine’ genes across the transcriptome. This demonstrates for the first time that sex-biased genes are indeed important in generating the sexual traits we observe in nature. Physical sex is determined by the combined action of many genes, some male-biased and some female-biased, and intermediate physical characteristics are possible simply through altering the expression of key sex-biased genes. This result has clear implications for how we view sex and gender in our own species, and greatly enhances our understanding of sexual selection and sexual dimorphism across the animal kingdom.

Original Article:

() PLOS Genetics

This research was made possible by funding from the European Research Council

Damage and Fidelity: The Role of the Female Germline in mtDNA Inheritance

Claire Asher11 November 2013

Billions of years ago, one single-celled organism engulfed another, beginning a symbiotic interaction that would change live on Earth forever. The mitochondria are what remains of this symbiotic event, and are responsible for producing energy in all eukaryotic cells. Derived from a free-living organism, they carry their own genes, but these genes are at risk of damage by a natural by-product of energy production – free radicals. Mitochondrial DNA in most cells are exposed to these reactive oxygen species and may be damaged over time, resulting in some diseases of age. However, if damage occurs to the mitochondrial genes in egg and sperm cells, this damage would be passed on to the next generation. Despite this, aging is not heritable, and very few mitochondrial mutations are passed from one generation to the next. Researchers in GEE have been investigating the mechanism responsible for this apparent paradox – mitochondrial inactivation – and have discovered that this mechanism is extremely widespread in the animal kingdom.

The mitochondria are the powerhouses of the cell, generating energy through oxidative phosphorylation down an electron transport chain. The electron transport chain occurs across the mitochondrial membrane, and was a key innovation during the evolution of multicellular life. Mitochondria originated as free-living single celled organisms that were engulfed inside another cell and subsequently formed a cooperative partnership that allowed cells to produce energy more efficiently. Because of their symbiotic origin, mitochondria brought an entire genome with them, and although this has been wittled down to only a small number of genes, some genes still reside inside the mitochondria. This is a big problem, however, because in the process of producing energy, mitochondria also produce harmful reactive oxygen species (ROS), also known as free radicals. These can cause mutations in DNA, and the mitochondrial genes are therefore at great risk because of their proximity to the site of ROS production. Mutations in mitochondrial DNA are thought to be a key cause of age-related diseases.

The Electron Transport Chain
Image by Rozzychan, creative commons.

Mutations in DNA (mitochondrial or nuclear) in most cells in the body can be harmful to the health of the individual, but will have no influence on the next generation. The genes which we pass onto the next generation are separated off during early development into special ‘germ line’ cells which form sperm and eggs. Great care is taken to minimise the risk of mutation to these genes – genes in germline cells act as a blue print for the next generation. This is essentially why aging is not heritable, and it is a system that works pretty well.

Sperm Cells
Image by be_sperm

However, sperm and egg cells need mitochondria to produce energy, and so mitochondrial genes in our germ cells may still be at risk of mutation. If the free radicals generated in germ-line mitochondria harm mitochondrial DNA, these damages would be passed on to the next generation! Research in GEE has uncovered a rather elegant solution to this problem – those mitochondria that will be passed to the next generation are maintained in an inactive state. It’s a bit like buying two toasters and keeping one in a cupboard, unused, to provide a template from which to build a new toaster when the old one breaks.

Mitochondria are only inherited through the maternal line – every mitochondria in your body came from your mother, and this is true for most animal species. The mitochondria in sperm are generally discarded at some point prior to fertilisation. So, in order to preserve the fidelity of mitochondrial DNA passed on to the next generation, we only need to ‘switch-off’ mitochondria in egg cells. This is great, since sperm really need their mitochondria to provide energy for all that swimming!

Egg Cell

Previous research by John Allen and colleagues in GEE indicated that mitochondria in egg cells of the moon jellyfish (Aurelia aurita) are inactive compared to mitochondria in sperm and somatic tissues. Recently, GEE’s Prof John Allen, along with Wilson de Paula (Queen Mary University of London) and colleagues have investigated this phenomenon further and discovered that this system of mitochondrial inactivation is widespread across the animal kingdom. Using qPCR, a technique for measuring and comparing expression patterns of specific genes, they found that in both fruit flies (Drosophila melanogaster) and zebrafish (Danio rerio) expression of three key respiratory genes (nad1, cob & cox1) is much lower in mitochondria in oocytes (egg cells) than in sperm and active muscle tissue. Expression levels were 15-fold lower in eggs, whereas sperm and muscle showed similar levels of expression. They also found that membrane electrical potential, a measure of the activity of the electron transport chain, was reduced in oocytes compared to both sperm and the surrounding tissue. Further, ROS production was 50- and 100-fold lower in the eggs of fruit flies and zebrafish respectively. Finally, they confirmed that oocyte mitochodria in both species exhibit a simpler structure, indicative of reduced activity. So, it seems that in both fish and flies, the mitochondria in egg cells represent little more than a blueprint, ready to be passed on to the next generation error-free. By deactivating ovarian mitochondria, the fidelity of information is ensured across generations, and aging is not heritable.

Wilson de Paula and Prof John Allen have now identified a similar pattern of mitochondrial inactivation in species across the animal kingdom, including jellyfish, fruitflies and zebrafish. Early in multicellular evolution, animals branched into two key groups distinguished by differing patterns of embryonic development; protostomes (including arthropods, molluscs and nematodes) develop their mouth first, whereas deuterostomes (including vertebrates, tunicates and starfish) develop their anus first. This seemingly small difference represents a fundamental divide in the animal kingdom. This study therefore demonstrates that mitochondrial inactivation occurs in both of these key branches. Previous work by de Paula and Allen has shown a similar pattern in jellyfish, members of the phylum Cnidaria which pre-date the great protostome-deuterstome divide. Together, this work suggests that mitochondrial inactivation, as a mechanism to ensure fidelity of mitochondrial DNA transmission across generations, is likely to have emerged early in the evolution of multicellular life on Earth.

Ensuring the faithful transmission of genes to the next generation is a key problem for all life on Earth. Although the mitochondrial symbiosis event which marked the emergence of eukaryotic life was a major breakthrough in efficient cellular energy production, it brought problems of its own. Mitochondria must carry a few genes in order to maximise responsivness to cellular demands, but these genes are at risk of damage from a natural by-product of energy production – free radicals. A system of mitochondrial inactivation in female germ cells (eggs) may serve to resolve this conundrum, and seems to be shared across all animal life.

Original Article:

() Genome Biology and Evolution

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

Size Matters: Why Reduced Sexual Ornaments are Rarely Seen

Claire Asher29 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)