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Competitive Generosity Drives Charitable Donations

By Claire Asher, on 17 April 2015

Unconditional generosity is a characteristic of humans on which we pride ourselves, and billions of dollars is donated to hundreds of thousands of charitable organisations every year. But look at it from an evolutionary perspective, and this trait seems difficult to explain. In some situations, giving may have evolved to advertise positive characteristics of the giver in the aim of attracting a mate. Recent research from GEE suggests this may explain the charitable behaviour of men donating to female fundraisers online. Data from over 2500 fundraising campaigns showed that men donate £10 more on average if previous male donors have been particularly generous.

Helping others at random, with no promise of reciprocity in the future, should not be favoured by natural selection as it will tend to disadvantage the altruist. Yet we see people doing just that every day. One theory that may explain selfless, unconditional generosity in humans (and other animals) is the ‘competitive helping’ hypothesis, which suggests generosity may sometimes be used to advertise positive characteristics to potential mates. The hypothesis suggests that people will compete to be the most generous, particularly when they are in the presence of attractive potential mates. If generosity is costly, and competition for mates is tough, then competitive generosity could be favoured by natural selection as a mechanism to honestly communicate quality. Only the best quality males could afford to be so generous, making them more attractive to on looking females.

To test this hypothesis, GEE researcher Dr Nichola Raihani and Professor Sarah Smith from the University of Bristol reviewed 2561 online fundraising pages, and selected 668 that had public donations and an image of the fundraiser. They then calculated the average donation running up to a large donation of £50 or more. They compared these donations with those made after the large donation, according to the gender of the donors and the gender and attractiveness of the fundraiser. They found men tended to give larger amounts after other men had made large donations. Men were also more generous when the fundraiser was an attractive female, giving four times more to female fundraisers following a large donation from another male. Attractive female fundraisers received £28 more during these bidding wars than less attractive females and males!

Interestingly, while this pattern is clear in donations by men, the same is not true for women donating money online. This suggests that male charitable behaviour represents a competitive helping display, favoured by sexual selection as an honest signal of male quality.

It’s fascinating that evolutionary biology can offer insights into human behaviour even in the modern world. People are really generous and their reasons for giving to charity are generally not self-serving but it doesn’t preclude their motives from having evolved to benefit them in some way. Take eating for example, our primary drive is to dispel the feeling of hunger, which is pleasurable, but the evolutionary purpose is to make sure we don’t starve and die. Generous behaviours can be seen in a similar way – the motivation for performing them doesn’t have to be the same as the evolutionary function.” – Dr Nichola Raihani

Original Article:

() Current Biology

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This research was made possible by funding from the Economic and Social Research Council (ESRC) and the Royal Society.

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

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

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

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

By Claire Asher, on 25 June 2014

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

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

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

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

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

A Male Red Jungle Fowl

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

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

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

Original Article:

() Proceedings of the Royal Society B

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

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

By Claire Asher, on 12 June 2014

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

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

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

Photograph of a male stalk-eyed fly.

A Male Stalk-Eyed Fly (Teleopsis dalmanni)

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

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

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

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

Photograph of Stalk-eyed flies, (Teleopsis dalmanni)

Stalk-eyed flies, (Teleopsis dalmanni)

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

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

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

Original Article:

() Heredity

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

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

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)

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

By Claire Asher, on 18 July 2013

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

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

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

Gene Expression and Sexual Dimorphism

Male and female Red Deer
(Cervus elaphus)

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

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

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

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

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

The fruit fly,
Drosophila melanogaster

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

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

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

Original Article:

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

Sexy Mates Ensure Survival in Stalk-Eyed Flies

By Claire Asher, on 30 May 2013

Attracting a female can be expensive, and females may use this cost to weed out poor quality males. Male ornaments such as antlers are a reliable indicator of nurture, but what about nature? Recent research into in male ornamentation in stalk-eyed flies reveals a key role for genetics, and highlights the importance of mate choice in species survival.

Males throughout the animal kingdom go to some weird and wonderful lengths to try and attract females. This might involve an elaborate dance, a carefully wrapped gift, or an ornate head-dress, and these adverts are often costly to the male who performs them. A peacock’s tail makes him conspicuous to predators; a red deer’s antlers require food and energy to grow. And a female finds all of this very sexy, because it informs her about the quality of the male; only the highest calibre males can afford the handicap.

Stalk-Eyed Flies
This phenomenon isn’t limited to birds and mammals, of course, even flies need to attract a mate, and stalk-eyed flies have a rather odd form of ornamentation: their eyes sit on the end of long stalks that protrude out horizontally from their head. Clearly this makes their lives difficult; long eye stalks take more energy to grow, and make the males more cumbersome during flight. So why do males grow these impractical eye stalks? Because, despite the costs, males with longer stalks have more luck with the ladies.

D. meigenii

A male Stalk-Eyed Fly (D. meigenii)
Photography by

Females are thought to be attracted to males with longer stalks because they are reliable indicators of the quality of the male. Males with good genes, who grew up in plentiful environments, produce the largest ornaments and consequently get their pick of the ladies. In other words, these traits are strongly dependent on environmental conditions (e.g. food availability, temperature) and genetics. Or so the theory goes. There is good evidence that the appearance of male sexual traits is influenced by the environment in which the male grew up, but few empirical tests have been conducted to see whether ornaments also reflect genetic quality. And until recently, we had little idea of what impact this might have at the population level.

Nature and Nurture
Recent research in GEE has taken a major step towards answering these questions. Bellamy and colleagues conducted a long-term inbreeding experiment with the African stalk-eyed fly (Diasemopsis meigenii) to investigate how eye stalk length is influenced by genetic stress. Inbreeding is known to be harmful to populations, causing inbreeding depression by increasing the frequency of rare and damaging mutations, and thereby reduce the fitness of individuals. If long eye stalks are a sign of high genetic quality, then we would expect inbreeding to reduce the size of eye stalks over time. And this is just what 11 generations of mating with siblings: eye span decreased significantly during the experiment, more so than other traits such as wing size, which are not considered sexy. Thus, male traits important for attracting a female are more sensitive to genetic quality than non-sexy traits, supporting previous theory about why females are attracted to these traits in the first place.

Surviving the Genetic Storm
One rather unexpected result, however, was that male eye span at the start of the experiment was also a strong predictor of whether the line went extinct or not before the end of the experiment. Less than half the original lines survived the entire 11-generation experiment, and those who did survive were descended from males with longer eye-stalks. This again supports the idea that male eye span in stalk-eyed flies is linked closely to genetic quality; males with long eye stalks carried fewer deleterious mutations when the experiment began and so were more robust against inbreeding depression and less likely to go extinct. This result may have intriguing implications for conservation and for population dynamics in general. It shows that individual decisions such as mate choice may influence the fate of a whole population. Conservationists should take mate choice and sexual selection into account when designing programmes to conserve species, especially those with small or declining populations.

Original Article:

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