Sloths, as we know and love them, are small, slow-moving creatures found in the trees of tropical rainforests. But modern sloths are pretty odd compared to their extinct relatives. Sloths (Folivora) are represented today by just six species in two families; the Megalonychidae (two-toed sloths) and the Bradypodidae (three-toed sloths). But 20,000 years ago there were perhaps as many as 50 species of sloth spread across the globe, and most were relatively large, ground-dwelling animals quite unlike modern sloths. While most modern sloths weigh in at a modest 6kg, extinct species such as Megatherium americanum and Eremotherium eomigrans could weigh up to 5 tonnes!
Archive for the 'Evolutionary Genetics' Category
From bread to beer, yeast has shaped our diets and our recreation for centuries. Recent research in GEE shows how humans have shaped the evolution of this important microorganism. As well as revealing the evolutionary origins of modern fission yeast, the new study published in Nature Genetics this month shows how techniques developed for detecting genetic causes of disease in humans can be usefully applied to better understand the ecology, biochemistry and evolution of commercially and scientifically important microorganisms like yeast.
Fission yeast, Schizosaccharomyces pombe, is one of the principal ‘model’ species that cell biologists use to try and understand the inner workings of cells. Most famously, Paul Nurse used this yeast to discover the genes that control cell division. The laboratory strain was first isolated from French wine in 1924, and has been used ever since by an increasingly large community of fission yeast researchers. However, serendipitous collection of new strains has continued slowly since that time, and many of these are associated with human fermentation processes – different strains have been isolated from Sicilian vineyards, from the Brazilian sugarcane spirit Cachaça and from the fermented tea Kombucha. Despite it’s enormous scientific importance, little is known about the ecology and evolution of fission yeast.
Research published this month by Professor Jürg Bähler, Dr Daniel Jeffares and colleagues from UCL’s department of Genetics, Evolution and Environment, along with researchers from 10 other institutions across five countries, reveals an intimate link between historic dispersal and diversification in yeast and our love of fermented food and drinks. The project sequenced the genomes of 161 strains of fission yeast, isolated in 20 countries over the last 100 years, enabling the researchers to reconstruct the evolutionary history of S. pombe, as well as investigating genetic and phenotypic variation within and between strains.
Beer, Wine and Colonialism
Bähler and Jeffares were able to date the diversification and dispersal of S. pombe to around 2,300 years ago, coinciding with the early distribution of fermented drinks such as beer and wine. Strains from the Americas were most similar to each other, and dated to around 1600 years ago, most likely carried across the Atlantic in fermented products by European colonists. This is reminiscent of findings for the common bread and beer yeast species, Saccharomyces cerevisae, whose global dispersal is thought to date to around 10,000 years ago, coinciding with Neolithic population expansions. This research therefore reveals the intimate link between human use of yeast for fermentation and it’s evolutionary diversification, and highlights the power of humans to shape the lives of the organisms with which they interact.
From Genotype to Phenotype
The researchers also used genome-wide association techniques to investigate the relationship between genotype and phenotype in the different strains. They began by carefully measuring 74 different traits in representatives of each strain. Some traits were simple, such as cell size and shape, but the researchers also measured environment-genotype interactions, for example by investigating growth rates and population sizes with different nutrient availabilities, drug treatments and other environment variables. In total, they identified 223 different phenotypes, most of which were heritable to some extent. Further, relatively few of the phenotypes were strongly linked to a particular population or region, making yeast ideal for genome-wide association studies (GWAS), unlike Saccharomyces cerevisae, for which it has not been possible to use GWAS successfully.
GWAS was developed to identify genes that are linked to specific diseases in humans, however this study highlights how the technique can usefully be applied to understanding evolution and genotype-phenotype relationships in other organisms. Tightly controlled experimental conditions that can be achieved with microorganisms in the laboratory make GWAS possible and informative for organisms such as yeast. The researchers found 89 traits that were significantly associated with at least one gene; the strongest association explained about a quarter of variation between individuals.
Hallmarks of Selection
Looking at variation in genomic sequence between strains also allowed the researchers to investigate which parts of the genome have undergone more evolutionary change than others, and which regions are likely to be particularly important for function. Genes and genomic regions that are crucial to survival (such as those involved in basic cellular function, for example), tend to change relatively little over evolutionary time, because most mutations in their sequence would be severely detrimental to survival. A process known as purifying selection tends to keep these genetic sequences the same over long stretches of evolutionary time. Less crucial genetic sequences have more freedom to change without having serious consequences; they are not subject to strong purifying selection and tend to show more variation between individuals and populations.
The authors found that genetic variation between strains was lowest for protein-coding gene sequences (those that produce protein products such as hormones and enzymes), which is to be expected. However, they found variation was also low in non-coding regions near genes. These regions are thought to be important in gene regulation, echoing an increasing appreciation that the evolution of the regulation of gene expression may be as important, if not more so, than the evolution of the gene sequences themselves.
This ground-breaking research from GEE reveals fascinating insights into the ecology and evolution of fission yeast, a microorganism that directly or indirectly influences our lives on a daily basis. It highlights how important humans have been in shaping the genomes of commercially and scientifically important organisms, whilst also expanding our knowledge of genes, genomes and phenotypes more generally. Applying techniques such as this to a wider range of organisms has the potential to vastly increase our understanding of the genomic dynamics of evolutionary change.
This research was made possible by funding from the Wellcome Trust, the European Research Council (ERC), the (BBSRC), the UK Medical Research Council (MRC), Cancer Research UK, the Czech Science Foundation and Charles University.
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?
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.
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.
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.
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.
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)
Why some regions or habitats contain vast, diverse communities of species, whilst others contain only relatively few species, continues to be the subject of scientific research attempting to understand the processes and conditions that allow and adaptive radiation. The Great African Lakes exist as freshwater ‘islands’, with spectacularly high levels of biodiversity and endemism. They are particularly famous for the hyperdiverse Cichlid fish, but they are also home to diverse assemblages of many other fish, such as catfish. Recent research in GEE investigated the evolution of Clatoteine catfish in Lake Tanganyika, to investigate the forces driving evolutionary radiations in the Great African Lakes. Their results suggest that evolutionary time is of key importance to catfish radiations, with recently colonised groups showing less diversity than long-standing species.
Lake Tangayika is the World’s second largest freshwater lake, covering 4 countries in the African Rift Valley (Tanzania, the Democratic Republic of the Congo, Burundi and Zambia). It is home to the highest diversity of lake-dwelling catfish on Earth, however the evolutionary history of these catfish is not fully understood. GEE academic Dr Julia Day and PhD Student Claire Peart, in collaboration with colleagues at the Natural History Museum, London and the South African Institute for Aquatic Biodiversity, investigated the evolutionary history of nocturnal Claroteine catfishes in Lake Tangayika. This group of catfish offers an excellent opportunity to investigate the influence of different factors in evolutionary diversification, as it includes multiple genera with varying range sizes and habitat types.
The Drivers of Diversification
Previous research has suggested a number of factors that are important in enabling adaptive radiations that can produce extremely high levels of biodiversity – deep lakes that experience lots of sunlight tend to favour evolutionary diversification. Diversification is also more common for species that have had a lot of evolutionary time in which to diverge and that experience high levels of sexual selection. Interestingly, although lake depth is important, the total size of the lake does not appear to be so important for diversification. A large geographical area to diversify into may influence the duration of adaptive radiations, however, with river-dwelling species showing more consistent species-production through time. This data suggests that adaptive radiations may be, to some extent, predictable, however much previous work has focussed on key model groups such as the Cichlid fish, and these hypotheses need to be generalised to other species and locations.The authors sequenced nuclear and mitochondrial genes from 85 catfish covering 10 of the 15 species of Claroteine catfish, in order to construct an evolutionary tree for the sub-family. Estimates of the relationships between species and the evolutionary timescales of colonisation and divergence allowed the authors to distinguish between the possibilities of single or multiple colonisation events, and the processes driving diversification. The results indicated that most Claroteine catfish in Lake Tangayika originate from a single colonisation of the lake between 5 and 10 million years ago, followed by evolutionary radiations to produce the variety of species present today. One species, Chrysichthys brachynema was the exception to this rule, having independently colonised the lake around 1 – 2 million years ago. This species has not shown adaptive radiation since colonisation, probably because of the relatively short time it has been present in the lake. These results support previous work that has suggested that time is an important factor in producing highly diverse species assemblages.
This research was made possible by funding from the Natural Environment Research Council (NERC), the National Council for Scientific and Technological Development (CNPQ), the National Geographic Society, and the Percy Sladen Memorial Trust Fund.
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).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.
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.
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.
There are two main hypotheses for how the extraordinarily high levels of endemism arose on the montane forest ‘islands’:
- 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.
- 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.
This research was made possible by funding from the Natural Environment Research Council (NERC).
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.
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.
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.
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.
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.
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.
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.
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.
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.
You’ve probably never given much consideration to why there are men and women. Or, more specifically, why there are two sexes, rather than one, three or 50. But this is a question that has been keeping some scientists awake at night for decades. Recent research in the department of Genetics, Evolution and Environment used mathematical models of evolution to investigate how the evolution of the two sexes was influenced by the inheritance patterns of the energy-producing organelle, mitochondria. The results of this model contradict previous work supporting the idea that inheritance of mitochondria through only one parent might explain the emergence of two sexes. The evolutionary dynamics of mitochondrial inheritance are more complex than previously thought.
Sexual reproduction is a beneficial thing, in evolutionary terms, but this benefit doesn’t depend upon there being different sexes, only on there being two individuals sharing their genes to produce an offspring. This system would also work with no sexes at all (everyone can mate with everyone), or with many sexes. In fact, two is actually the worst number you could have picked – with two sexes any individual is limited to an available pool of mates just 50% of the population. With three sexes, this pool would increase to 66% of the population, with four 75%, and so on. So why have most sexually-reproducing species on settled on two sexes?
In a few previous GEE blog articles (see here and here), I have discussed the phenomenon known as ‘uniparental mitochondrial inheritance’ (UPI), in which mitochondria, organelles found in our cells that are responsible for generating energy, are inherited only through the maternal line – that is, you inherit all of your mitochondria from your mother and none from your father. UPI is found in many living things, although some species do things a bit differently and there are many different ways to achieve the same result. Work by GEE researcher Professor John Allen has previously shown that the mitochondria within egg cells in jellyfish, fruit flies and fish are largely inactive; this inactivity allows for a perfect ‘mitochondrial template’ to be passed on to the offspring and prevent the accumulation of mutations through the generations. Essentially, this is why aging isn’t heritable. It wouldn’t work to inactivate sperm mitochondria because they need so much energy for all that swimming, so if we did inherit mitochondria from our fathers they would probably be mutated. UPI is also thought to help evolution remove harmful mutations from the population and reduce conflict and promote coadpatation between the mitochondrial symbiont and its host cell.
So, UPI makes a lot of sense, evolutionarily, and some scientists think it might also explain why we have two sexes, as opposed to any other mating system. It’s important to be clear, when we talk about having two sexes we’re saying nothing about the external differences between the sexes (sexual dimorphism) observed in many multicellular organisms. We’re talking about the existence of two ‘mating types’, such that individuals cannot mate with members of the same type. Recent research by another group of GEE academics including Professor Andrew Pomiankowski, Dr Nick Lane and Professor Robert Seymour, investigated the evolution of UPI and in particular it’s relationship with the evolution of a two-sex mating system. We might expect a strong link between UPI and the existence of two sexes, since uniparental inheritance immediately generates differences between the two mating partners, and ensures that reproduction is not possible unless one member of each ‘type’ is present. Although UPI is often thought to have been a key driver in the evolution of mating types, there have been few investigations of what conditions are needed for the fitness benefits of UPI to actively drive the emergence of two mating types. So the authors developed a new mathematical model of mitochondrial inheritance and the evolution of UPI in a population where biparental inheritance (BPI) is the norm. They incorporated mitochondrial mutation (which might sometimes be selfish) and selection into the model, and included different mating types.
The model agreed with a great deal of previous work that indicates that UPI tends to increase fitness. It does so slowly, with selection acting cumulatively across many generations to remove less fit mitochondrial variants and increase fitness for UPI individuals. In a population of individuals where mitochondria is inherited biparentally, a new mutation causing UPI exists in a single individual. Slowly UPI improves the fitness of cells by reducing the number of mutated mitochondria they carry, and the UPI mutation might start to spread in the population. The problem is, as it spreads the benefits of UPI are inevitably leaked into the rest of the BPI population – UPI individuals mate with BPI individuals producing some BPI offspring who carry the fitter mitochondria from their UPI parent. This leaking of benefits means that the fitness benefits of UPI are frequency-dependent; the more common UPI becomes in a population, the less each UPI individual benefits from the reproductive strategy. This makes it hard for UPI to fully take over a population – their model tended instead to produce mixed populations with some UPI and some BPI individuals interbreeding.
If the researchers included mating types in the model at the start of it’s evolutionary run, then UPI could become associated with specific mating types and in this situation, so long as mutation rates were high or each cell carried many mitochondria, UPI could spread to fixation in the population. But UPI itself was not able to alter the number or existence of mating types. The authors suggest that this may explain the continuum of UPI levels we observe in nature. For any given species, the occurrence of UPI will depend upon the evolutionary starting point, energetic demands, mutation rates and the selfish (or unselfish) nature of mutations.
Although most people never even consider why we have two sexes, male and female, the evolution of a two mating-type system is seemingly paradoxical and many theories and hypotheses have been proposed to explain it. One such explanation is that uniparental inheritance, which is critical for stabilising the mitochondria-cell symbiosis and preventing the accumulation of harmful mutations, may have driven the evolution of two sexes. However, mathematical modelling by scientists in GEE suggests this is not the case, and UPI more likely evolved after the two mating-type system emerged. In their model, although UPI initially spreads through populations, it’s fitness benefits are frequency-dependent, meaning it only rarely takes over an entire population. Populations in which all members inherit mitochondrial uniparentally are only possible when a mutation causing UPI becomes tighly linked to genes that determine mating type. The initial emergence of two mating types still requires an explanation independent from mitochondrial inheritance patterns.
This research was made possible by funding from the Natural Environment Research Council (NERC), the Engineering and Physical Sciences Research Council (EPSRC) and the Leverhulm Trust.
Size matters. Particularly when it comes to finding a mate. Across the animal kingdom, body size plays a crucial role in determining how successful individuals are at surviving and reproducing. Large males are often better at fighting off competing males, while large females generally produce more offspring. However, being big isn’t always best. In some environments, small individuals may have a better chance of survival. Choosing a partner the right size may help to ensure a good start in life for your offspring. Recent research in GEE suggests that even simple organisms such as yeast are able to choose the best size mate to ensure their offspring survive and reproduce.
In single-celled organisms, just like their multicellular counterparts, the ideal body size depends on surrounding conditions in the environment. In nutrient rich environments, larger cells do better, whilst in nutrient poor environments, smaller cells prevail. In many multi-cellular animals, females have been shown to select mates based on body size to ensure their offspring the best possible chances of survival. Are unicellular organisms also able to make these kinds of selections? A recent paper by GEE Researchers Dr Carl Smith, Prof. Andrew Pomiankowski and Dr Duncan Greig investigated this phenomenon in yeast.
The Curious Life-Cycle of Yeast
Yeast, being single-celled, are able to reproduce asexually – budding off a new copy of themselves. However, when times are hard, yeast can also enter a sexual phase of reproduction. When nutrient levels are low, a yeast cell will divide into sexual spores. These spores are haploid, carrying only one copy of each chromosome (rather than the usual two), making them analogous to sperm and egg cells. Spores will remain dormant until they sense an improvement in the environment, at which point they spring into action and try to find a mate. Spores come in two mating types and must always mate with another spore of the opposite type – a system based on mating pheromones released by spores to attract the opposite sex.
Body size is important in both the asexual and sexual phases of yeast reproduction. Yeast cells must reach a certain critical size before they can bud asexual copies of themselves, although this critical size is smaller in poorer environments. Likewise, during sexual reproduction, the cell size of the offspring is determined by the cell size of the two spores that fuse together. GEE researchers first investigated how body size influenced reproductive success in both phases of yeast reproduction. Cell size was an important influence on how quickly spores awoke from dormancy to begin searching for a sexual partner; large spores became active 38% more quickly in a nutrient-rich environment, whereas smaller spores were 63% faster when conditions were poor. Asexual reproduction was similarly affected, with large spores budding off asexual copies sooner in good environments and small spores budding sooner in bad environments. Size matters when it comes to yeast reproduction, but bigger isn’t always better.
Are Sexual Yeast Cells Selecting the Right Sized Partner for their Environment?
To answer this question, GEE Researchers created a mating-choice experiment, in which a haploid yeast cell of one mating type is presented with two cells of the opposite type, one small and one large. To mate, two of these haploid cells will fuse to form a single, diploid cell which can resume asexual reproduction. These experiments were performed with different sizes of focal yeast cell, and in different environments, to see whether the focal cells were able to select the best partner – one that would give the final fused cell the best chance of survival. This is a critical choice – mating in these single-celled organisms is an irreversible decision, the size of the ‘offspring’ cell is directly determined by the size of the two haploid cells that fuse, and cell size will influence how quickly the ‘offspring’ can reproduce.
The results of the experiment indicate that yeast cells are indeed able to make careful calculations about their choice of partner and select the one closest to the optimum size for the environment. In nutrient rich environments, yeast cells tended to select larger mates, whereas in poorer environments they tended to select smaller mates. This was true regardless of their own body size, indicating that cells were not simply mating with similar sized partners, but making a choice based upon the mates available and the environment around them. The authors suggest that such seemingly complex behaviour could be generated quite simply – if cells that are better adapted to their environment begin emitting these pheromones earlier, or produce them in larger amounts, they would be more easily detected by a prospective mate.
Size is a crucial determinant of success, survival and reproduction for most living organisms. However, the optimum size often depends upon environmental conditions, as GEE researchers have shown to be the case for yeast. For most organisms, selecting a mate is an important decision that will influence the success of their offspring. For yeast even more so, this decision is critical, as it is irreversible. A new paper from GEE researchers shows that yeast cells also consider the quality of their partner when mating. During sexual reproduction, yeast cells are able to select a mate of the optimum size for the environment, thereby improving the chances that the resulting offspring cell will reproduce.
This research was made possible by funding from the Natural Environment Research Council (NERC), the Biotechnology and Biological Sciences Research Council (BBSRC), the Engineering and Physical Sciences Research Council (EPSRC), The Royal Society and the Max Planck Society.