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Archive for the 'Evolution and Development' Category

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.

Male Promiscuity Boosts Role of Chance in Sex Chromosome Evolution

By Claire Asher, on 19 March 2015

Humans, like all mammals and birds, determine sex with chromosomes. Whether a fertilised egg develops into a male or female depends on what chromosomes it carries Scientists have long recognised that genes evolve a little differently on the sex chromosomes, and recent research in GEE suggests this may be due to differing patterns of inheritance that favour the influence of chance on gene sequence change. Furthermore, promiscuity in males has a large influence on the magnitude of this effect, with chance playing an even greater role in sex-chromosome evolution in highly promiscuous species. Using genetic sequence data in combination with physical and behavioural measurements of promiscuity in birds, Dr Alison Wright and Professor Judith Mank report strong evidence for the role of neutral forces in sex chromosome evolution.

In birds and mammals, along with some invertebrates and reptiles, sex is determined by the chromosomes you carry – the sex chromosomes, as they are aptly named. If you are a male mammal, you carry one X and one Y chromosome; a female mammal carries two X chromosomes. Similarly, if you are a male bird, you carry two Z chromosomes; a female carries one Z and one W. Whether it’s the XY system, the ZW system or even the UV system used by some species of algae, the result is more or less the same. Sex is determined by the presence or absence of particular chromosomes. This isn’t always the case – some species determine sex using temperature during development, other species determine sex based on social conditions, while others do away with fixed sexes altogether and are either hermaphrodite or possess the ability to switch sex. However, one of the most common, and certainly the best studied, systems among living organisms is to determine sex with chromosomes.

Unlike autosomal chromosomes (all our chromosomes that are not sex chromosomes), sex chromosomes are not inherited and expressed equally across the sexes. The Y and W chromosomes only ever appear in one sex, for example. This has some interesting consequences for evolution. For example, scientists have found that the ‘major sex chromosomes’ (X and Z chromosomes) tend to evolve faster than the autosomes. Known as the Faster-X (or Faster-Z) effect, this phenomenon is now well documented in a range of different species, and scientists have suggested a number of possible explanations for why this might be the case. Faster evolution on the major sex chromosomes might be caused by more effective natural selection favouring beneficial mutations (adaptive hypothesis) or due to less effective natural selection failing to remove harmful mutations (neutral hypothesis).

Why would natural selection act differently on sex chromosomes than autosomal ones? In a paper published in Molecular Ecology this month, Dr Alison Wright explains that the differences between chromosomes arise because of differences in the pattern of inheritance, which ultimately influences the number of chromosomes that are passed on to the next generation, called the effective population size. An individual who never reproduces is an evolutionary dead end, and as their genes are not passed on, and they are not counted in the effective population size. Individuals that do mate contribute sex chromosomes unevenly, and this can have a significant impact on the course of sex-chromosome evolution.

When two individuals mate, they each pass one of each pair of chromosomes to the offspring. Each chromosome has an equal likelihood of being carried by the offspring, and the effective population size (ie chance of being passed on) of all autosomal chromosomes is the same. But for the sex chromosomes, things are a bit more complicated. Each time a pair of individuals mate, between them they bring three major sex chromosomes and one minor chromosome to the table. This translates to major sex chromosomes having an effective population size three times larger than the minor sex chromosomes. And both sex chromosomes have a smaller effective population size than the autosomes.

But that’s only if everybody is monogamous. As soon as promiscuity is involved, things get even more complicated. If males are promiscuous (and they often are, in the animal kingdom), then this means some males in the population are likely to be very successful, while others fail to reproduce at all. In other words, the variance in male mating success is much higher. Promiscuity reduces the effective population size of the minor chromosomes even further.

promiscuitysexchromosomes

Why does effective population size matter? Well, the effective population size determines the relative influence of chance on gene sequence evolution. Although we generally think of evolution progressing as natural selection favours beneficial mutations and purges deleterious ones, chance also has a big role to play. Chance, known in this context as genetic drift, has a bigger impact on small populations, and rare mutations. This is because when a particular mutation is rare, it only takes a little bit of bad luck for it to be lost forever. Just think of the times you’ve walked home in the rain only to hear the characteristic crunch of the end of a snail’s life – here your foot is the agent of genetic drift. The death of that snail had little or nothing to do with the genes it carried, but your foot has altered the course of evolution, slightly. The effective population size of autosomal genes reflects the population size of the organisms they are found in, but for the sex chromosomes, their effective population size is even smaller, making them more prone to genetic drift.

Dr Alison Wright, Professor Judith Mank and colleagues from GEE sequenced expressed genes in six species of birds, spanning 90 million years of evolution, to investigate the rate of evolutionary change in genes on different chromosomes. They compared sequence data from monogamous species like the Swan Goose (Anser cygnoides) and the Guinea Fowl (Numida meleagris) with promiscuous species like the Mallard duck (Anas platyrhynchos), wild Turkey (Meleagris gallopavo), and Peafowl (Pavo cristatus) to investigate how gene sequences and gene expression patterns vary both within and between species. They then matched data on the rate of evolution with characteristics of species that are associated with promiscuity, such as testes weight and sperm number. Their results indicate that natural selection is less effective on the Z chromosome in general, and this becomes even more pronounced in promiscuous species. The authors therefore conclude that Faster-Z evolution in birds is not adaptive, but is driven by neutral processes.

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Differences in gene sequences within and between species can tell us a lot about the rate of evolution for different lineages. This is because the genetic code has some redundancy in it – DNA is split up into three-letter words or codons, and there are many cases where different codons translate into the same amino acid. So, it is possible to have genetic sequence change that is essentially invisible to natural selection – it doesn’t alter the resulting protein sequence and so has no influence on the organism. Changes in gene sequence that swap between these ‘synonymous’ codons can therefore give us a rough baseline of neutral change. Non-synonymous differences (the ones that do have an effect on the organism), between individuals or between species, represent the rate of evolution. More non-synonymous changes suggests either positive selection, where evolution favours those changes because they are beneficial, or genetic drift, where selection is weaker and cannot remove slightly harmful mutations from the population. The authors found that genes on the Z chromosome show a faster rate of non-synonymous change than autosomal genes. Further, the ratio was significantly correlated with measures of promiscuity, with more promiscuous species having more non-synonymous changes.

Although this could be a mark of positive natural selection, the authors found no difference in the number of genes undergoing positive selection between sex- and autosomal-chromosomes, suggesting the Faster-Z effect is driven by genetic drift rather than positive selection. In fact, differences within species indicate that natural selection is less effective at removing mildly deleterious mutations from the Z chromosome than the autosomes. Combined with other analyses on gene expression, these results show strong support for the neutral explanation for Faster-Z evolution in birds.

Interesting, promiscuity increases the effective population size of X chromosomes, and that may explain why previous studies have found evidence that Faster-X chromosome may well be due to positive selection. These differences suggest that Z chromosomes may be less important in adaptation than X chromosomes.

Original Article:

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

Function Over Form:
Phenotypic Integration and the Evolution of the Mammalian Skull

By Claire Asher, on 8 December 2014

Our bodies are more than just a collection of independent parts – they are complex, integrated systems that rely upon precise coordination in order to function properly. In order for a leg to function as a leg, the bones, muscles, ligaments, nerves and blood vessels must all work together as an integrated whole. This concept, known as phenotypic integration, is a pervasive characteristic of living organisms, and recent research in GEE suggests that it may have a profound influence on the direction and magnitude of evolutionary change.

Phenotypic integration explains how multiple traits, encoded by hundreds of different genes, can evolve and develop together such that the functional unit (a leg, an eye, the circulatory system) fulfils its desired role. Phenotypic integration could be complete – every trait is interrelated and could show correlated evolution. However, theoretical and empirical data suggest that it is more commonly modular, with strong phenotypic integration within functional modules. This modularity represents a compromise between a total lack of trait coordination (which would allow evolution to breakdown functional phenotypic units) and the evolutionary inflexibility of complete integration. Understanding phenotypic integration and its consequences is therefore important if we are to understand how complex phenotypes respond to natural selection.

Functional modules in mammals, Goswami et al (2014)

Functional modules in mammals, Goswami et al (2014)

It is thought that phenotypic integration is likely to constrain evolution and render certain phenotypes impossible if their evolution would require even temporary disintegration of a functional module. However, integration may also facilitate evolution by coordinating the responses of traits within a functional unit. Recent research by GEE academic Dr Anjali Goswami and colleagues sought to understand the evolutionary implications of phenotypic integration in mammals.

Expanding on existing mathematical models, and applying these to data from 1635 skulls from nearly 100 different mammal species including placental mammals, marsupials and monotremes, Dr Goswami investigated the effect of phenotypic integration on evolvability and respondability to natural selection. Comparing between a model with two functional modules in the mammalian skull and a model with six, the authors found greater support for a larger number of functional modules. Monotremes, whose skulls may be subject to different selection pressures due to their unusual life history, did not fit this pattern and may have undergone changes in cranial modularity during the early evolution of mammals. Compared with random simulations, real mammal skulls tend to be either more or less disparate from each other, suggesting that phenotypic integration may both constrain and facilitate evolution under different circumstances. The authors report a strong influence of phenotypic integration on both the magnitude and trajectory of evolutionary responses to selection, although they found no evidence that it influences the speed of evolution.

Thus, phenotypic integration between functional modules appears to have a profound impact on the direction and extent of evolutionary change, and may tend to favour convergent evolution of modules that perform the same function (e.g bird and bat wings for powered flight), by forcing individuals down certain evolutionary trajectories. The influence of phenotypic integration on the speed, direction and magnitude of evolution has important implications for the study of evolution, particularly when analysing fossil remains, since it can make estimates of the timing of evolutionary events more difficult. Failing to incorporate functional modules into models of evolution will likely reduce their accuracy and could produce erroneous results.

Phenotypic integration is what holds together functional units within an organism as a whole, in the face of natural selection. Modularity enables traits to evolve independently when their functions are not strongly interdependent, and prevents evolution from disintegrating functional units. Through these actions, phenotypic integration can constrain or direct evolution in ways that might not be predicted based on analyses of traits individually. This can have important impacts upon the speed, magnitude and direction of evolution, and may tend to favour convergence.

Original Article:

() Global Environmental Change

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This research was made possible by support from the Natural Environment Research Council (NERC), and the National Science Foundation (NSF).

Evolving Endemism in East Africa’s Sky Islands

By Claire Asher, on 8 August 2014

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

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

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

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

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

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

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

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

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

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

Original Article:

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

It’s All in the Wrist

By Claire Asher, on 20 December 2013

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

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

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

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

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

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

Original Article:

() BMC Evolutionary Biology



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

The Transcriptional Profile of A ‘Wingman’

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

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

Skulls and Teeth: Constraints on Mammalian Evolution

By Claire Asher, on 7 June 2013

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

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

A Koala (Phascolarctos cinereus)
A Marsupial Mammal

Chipmunk

A Chipmunk (Neotamias umbrinus)
A Placental Mammal

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

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

Facial bones (viscerocranium)
and braincase (neurocranium)

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

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

Coloured teeth

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

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

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

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

Original Articles:

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

 

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