A A A

Handicaps, Honesty and Visibility
Why Are Ornaments Always Exaggerated?

By Claire Asher, on 23 October 2014

Sexual selection is a form of natural selection that favours traits that increase mating success, often at the expense of survival. It is responsible for a huge variety of characteristics and behaviours we observe in nature, and most conspicuously, sexual selection explains the elaborate ornaments such as the antlers of red deer and the tail of the male peacock. There are many theories to explain how and why these ornaments evolve; it may be a positive feedback loop of female preference and selection on males, or ornaments may signal something useful, such as the genetic quality of the male carrying them. One way or another, despite the energetic costs of growing these ornaments, and the increase risk of predation that comes with greater visibility, sexually selected ornaments must be increasing the overall fitness of individuals carrying them. They do so by ensuring the bearer gets more mates and produces more offspring.

Theory predicts that sexually selected traits should be just as likely to become larger and more ostentatious as they are to be reduced, smaller and less conspicuous. However, almost all natural examples refer to exaggerated traits. So where are all the reduced sexual traits?

Runaway Ornaments

Previous work by GEE researchers Dr Sam Tazzyman, and Professor Andrew Pomiankowski has highlighted one possible explanation for this apparent imbalance in nature – if sexually selected traits are smaller, they are harder to see. Using mathematical models, last year they showed that differences in the ‘signalling efficacy’ of reduced and exaggerated ornaments was sufficient to explain the bias we see in nature. Since the purpose of sexually selected ornaments is to signal something to females, if reduced traits tend to be worse at signalling, then it makes sense that they would rarely emerge in nature. Their model covered the case of runaway selection, whereby sexually selected traits emerge somewhat spontaneously due to an inherent preference in females. It goes like this – if, for whatever reason, females have an innate preference for a certain trait in males, then any male who randomly acquires this trait will get more mates and produce more offspring. Those offspring will include males carrying the trait and females with a preference for the trait, and over time this creates a feedback loop that can produce extremely exaggerated traits. Under this model of sexual selection, differences in the signalling efficacy can be sufficient to explain why we so rarely see reduced traits.

Handicaps

However, this is just one model for how sexually selected ornaments can emerge, so this year GEE Researchers Dr Tazzyman and Prof Pomiankowski, along with Professor Yoh Iwasa from Kyushu University, Japan, have expanded their research to include another possible explanation – the handicap hypothesis. According to the handicap principle, far from being paradoxical, sexually selected ornaments may be favoured exactly because they are harmful to the individual who carries them. In this way, only the very best quality males can cope with the costs of carrying huge antlers or brightly coloured feathers, and so the ornament acts as a signal to females indicating which males carry the best genes. This is an example of honest signalling – the ornament and the condition or quality of the carrier are inextricably linked, and there is no room for poor quality males to cheat the system.

Using mathematical models, the authors investigated four possible causes for the absence of reduced sexual ornaments in the animal kingdom. Firstly, like the case of runaway selection, differences in signalling efficacy might explain the bias. Under the handicap hypothesis, ornaments act as signals of genetic quality, so it would be little surprise that their visibility or effectiveness at conveying the signal would be important. Smaller ornaments may simply be worse at attracting the attention of females, meaning that the benefits of the sexual ornament don’t outweigh the costs. Similarly, the costs for females of preferring males with reduced ornaments may be higher than for exaggerated ornaments, because it is easier to find males with exaggerated traits. Again, this could theoretically tip the balance of cost and effect away from selecting for reduced ornaments. An alternative explanation is that the costs of the ornament itself are different for reduced and exaggerated traits. This seems quite likely in many cases, since a large ornament would require more resources to grow. But in this case selection would be more likely to produce reduced ornaments with lower costs! In order to replicate the excess of exaggerated traits we see in nature, reduced traits would have to cost more – much less biologically plausible. However, if large ornaments tend to be more costly, then they may be more likely to be condition-dependent, a key tenant of the handicap principle. Exaggeration may be more effective at producing honest signalling and exaggerated traits may therefore be more useful to females as a signal of quality.

Honest Signals

The results of modelling highlighted two key ways in which exaggerated traits might be favoured by the handicap process. In the model, when exaggerated traits have a higher signalling efficacy or are more strongly condition-dependent, exaggerated traits tend to be more extreme than reduced traits. The model still predicts that reduced traits are equally likely to evolve, just that they will tend to be less extreme examples of ornamentation. The other two possible explanations – higher costs to females that prefer small ornaments or the males that carry them, failed to consistently produce the observed lack of reduced ornaments. Both explanations were able to produce this outcome under certain circumstances, but in other circumstances they produced the opposite effect. Exaggerated ornaments, therefore, may be more common because they are more effective signals that are more likely to be honest.

Based on this and previous work by Dr Tazzyman and colleagues, asymmetries in the signalling efficacy of reduced and exaggerated traits is sufficient to explain the lack of reduced traits in nature. Whether ornaments evolve via runaway selection or the handicap process, asymmetrical signalling efficacy tends to favour exaggerated traits. However, in the case of the handicap process, asymmetries in condition-dependance of the trait may also be involved. These two explanations are not mutually exclusive, and it is likely that in reality many factors are involved.

Importantly, for both explanations and for both type of sexual selection, the models still predict that exaggeration and reduction will be equally likely. The differences emerge in terms of how extreme the ornament will become. Thus, this work predicts that there are many examples of reduced ornaments in nature, perhaps we just haven’t found them yet. This is especially likely if reduced traits that might be less noticeable anyway also tend to be less extreme. Alternatively, there may be other asymmetries not yet considered that make reduced ornaments less likely to emerge in the first place.

Where Next?

The authors suggest some very interesting avenues for future research. Firstly, they suggest that more complex models investigating how multiple different asymmetries may act together to produce sexually selected ornaments will get us closer to understanding the intricate dynamics of sexual ornamentation. Secondly, these models have only considered cases where evolution of the trait eventually settles down – at a certain ornament size, the costs and benefits of possessing it are equal, and the trait should remain at this size. However, in some cases the dynamics are more complex, and traits undergo cycles of exaggeration and reduction. Research into the impact of asymmetries in condition-dependence and signalling efficacy in these ‘nonequilibrium’ models would yield fascinating insights into the evolution of sexual ornaments.

Original Article:

() Evolution

nerc-logo-115ERCepsrc-lowres

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

Sex Differentiation Begins During Early Development

By Claire Asher, on 27 August 2014

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

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

The fruit fly,
Drosophila melanogaster

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

Juveniles Show Sex-Biased Gene Expression

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

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

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

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

Continuity and Sex Differences

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

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

The Rate and Form of Evolution

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

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

Original Article:

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

Further Reading:

ERC

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

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

By Claire Asher, on 25 June 2014

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

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

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

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

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

A Male Red Jungle Fowl

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

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

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

Original Article:

() Proceedings of the Royal Society B

nerc-logo-115new-bbsrc-colour

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.

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

By Claire Asher, on 6 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.

The Transcriptional Profile of A ‘Wingman’

By Claire Asher, on 27 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.
Figure_S1

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

By Claire Asher, on 11 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

By Claire Asher, on 29 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)

How Energy Shapes Life: Our Mitochondrial Partners

By Claire Asher, on 21 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