Research themes

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“Our research lies at the interface of development, ecology, and evolution. We use experimental and comparative methods, guided by mathematical modelling and conceptual analysis”

 

Inheritance and evolution

Everyone knows that parents provide more than DNA for their offspring. Development does, after all, start with an egg. But such mechanisms have been treated as parental ‘effects’ on offspring phenotype rather than as a mechanism of inheritance, a term that has been restricted to the transmission of genes. As a consequence, non-genetic sources of inheritance have not played a prominent role in discussions of how evolution works.

Most work – including our own – has instead focused on non-genetic inheritance as an adaptive outcome of evolution. For example, we could ask how parental and offspring plasticity co-evolve and if this enables non-genetic transmission of information between generations. We can also ask if incomplete epigenetic resetting between generations can be favoured by natural selection. We have addressed some of these issues using mathematical modelling, partly through of an FP-7 funded large collaborative project called IDEAL.

 

But non-genetic inheritance is more than an adaptation to transfer information between generations (or a cause of phenotypic variance that biases responses to selection as in many quantitative genetic models). We have suggested that we can gain a number of important insights from viewing heredity as a developmental process. This allows us to address the role of non-genetic inheritance in the origin, spread, and maintenance of phenotypic variation, a perspective that can motivate further theoretical and empirical research on the causes of evolution.

 

If you want to know more:

Uller, T., English, S. & Pen, I. 2015. When does natural selection favour incomplete epigenetic resetting in germ cells? Proceedings of the Royal Society of London B 282: 20150682

Uller, T. & Helanterä, H. Heredity in evolutionary theory. In Challenges to Evolutionary Biology: Development and Heredity (eds. P. Huneman & D. Walsh), Oxford University Press, forthcoming

Badyaev, A. V & Uller, T. 2009. Parental effects in ecology and evolution: Mechanisms, processes, and implications. Philosophical Transactions of the Royal Society, 364: 1169-1177

Plasticity and Evolution

Daphnia_magna-female_adultThe environment is, in Scott Gilbert’s words, ‘a normal agent of development’. The implications of this fact for the study of evolution are not obvious. We could treat all environmental responsiveness as genetically specified norms of reaction, shaped by natural selection, mutation, and drift. This is often useful if the aim is to predict when organisms are well served by developing different phenotypes in different environments, i.e., the evolution of adaptive plasticity. It is less useful if the aim is to understand the origin and evolution of the mechanisms of plasticity, and it does not explain the environmental dependence of phenotypes that are not adaptively plastic.

Plasticity can also be a cause, and not only a consequence, of evolution. In this scenario, the directionality of evolution is partly given by how organisms accommodate environmental change, with selection stabilizing these accommodations that show high functionality (i.e., are fit). How we best model this process remains unclear but we can make a number of predictions based on the relationship between plastic responses – their direction, mechanisms and so on – and patterns of adaptive divergence. We explore these problems in a number of projects in the group using a range of methods, from meta-analysis of published data to experimental analysis using different –omics methods.

 

 

If you want to know more:

Laland, K.L., Uller, T, Feldman, M., Sterelny, K., Müller, G.B., Moczek, A., Jablonka, E. & Odling-Smee, J. The extended evolutionary synthesis: its structure, core assumptions, and predictions. Proceedings of the Royal Society of London 282: 20151019

Uller, T. & Helanterä, H. Heredity in evolutionary theory. In Challenges to Evolutionary Biology: Development and Heredity (eds. P. Huneman & D. Walsh), Oxford University Press, forthcoming

Causes and Consequences of Hybridization

The branches of the tree of life sometimes exchange heritable material. Gene transfer via hybridization is increasingly recognized as an important source of diversification and adaptation. However, only rarely are systems sufficiently well understood to predict the degree and direction of hybridization, which limits our understanding of its causes and consequences.

We have therefore experimentally studied the extent, direction, and phenotypic determinants of hybridization upon secondary contact between sub-species of the common wall lizard, Podarcis muralis. These lineages are now in contact in three different contexts: (a) in a native hybrid zone; (b) following recent introduction of one lineage into the native range of the other, and (c) in non-native populations founded by animals of both origins.

 

wallies

hybrid charts

Our results show that sexual selection generates asymmetric introgression of both genes and phenotypes, with an increasing difference between neutral genetic markers and sexually selected characters. We are currently finishing the first phase of this project that used experimental studies to establish the causes and targets of sexual selection upon secondary contact. Ongoing research, funded by the Swedish Research Council, focuses on genome-wide studies of introgression using high-throughput sequencing to test how well our predictions from experimental work are supported at the level of genomes.

 

If you want to know more:

Heathcote, R., MacGregor, H., Sciberras, J., While, G.M., D’Ettorre, P. & Uller, T. Male behaviour drives assortative reproduction during the initial stage of secondary contact in lizards. Journal of Evolutionary Biology 29: 1003-1015

While, G.M., Michaelides, S., Heathcote, R., MacGregor, H., Zajac, N., Beninde, J., Perez I de Lanuza, G., Carazo, P., Sacchi, R., Zuffi, M.A.L., Horvathova, T., Fresnillo, B., Schulte, U., Veith, M., Hochkirch, A. & Uller, T. Sexual selection drives asymmetric introgression in wall lizards. Ecology Letters 18: 1366-1375

Adaptation in Alien Species

hatchlingIntroduced populations offer valuable systems to study evolution. Our main study system is the common wall lizard. This is a species from southern Europe that has been introduced many times in different locations in Europe and in North America. We have focused on non-native populations in England and established their origin, genetic diversity, and inbreeding. Small population size should limit the adaptive potential of these populations. However, it turns out that non-native lizards have, since their introduction some decades ago, taken a small adaptive step towards viviparity in the colder climate in England. This reduces the time needed for completing embryogenesis in the nest, which is very important since the cool soil in England means development sometimes is so slow embryos fail to hatch before autumn. But embryos also develop faster at cooler temperatures.

These responses help the wall lizards to persist north of their natural range. We are now interested in asking what the underlying mechanisms behind these responses are, if they are similar to those underlying adaptive divergence during natural range expansion, and if developmental bias facilitates rapid adaptation to climate.

 

If you want to know more:

While, G.M., Williamson, J., Prescott, G., Horvathova, T., Fresnillo, B., Beeton, N.J., Halliwell, B., Michaelides, S. & Uller, T. Adaptive responses to cool climate promotes persistence of a non-native lizard. Proceedings of the Royal Society of London B 282: 20142638

Michaelides, S., While, G.M., Zajac, N. & Uller, T. Widespread primary, but geographically restricted secondary, human introductions of wall lizards, Podarcis muralis. Molecular Ecology 24: 2702-2717

Ecology and Evolution of Social Complexity in Lizards

Ask someone to name a social animal and her thoughts are drawn to ants, meerkats, or humans. In contrast, the social life of lizards may seem dull. Not so. Some lizards live in social groups that differ in size and complexity in fascinating ways. Together with former postdoc Geoff While at the University of Tasmania we study links between behavior and social structure in a group of lizards known as Egernia.

egernia

 

Our main study species Liopholis whitii lives in family groups. Geoff has shown that the composition and stability of these groups are dictated by both the genetic structure of the population and the ecological conditions. Together these factors shape selection on a suite of characters that are important for understanding the social life of lizards. Egernia are also interesting because species differ in their social systems, ranging from solitary species to those that live in large groups with several overlapping generations. This makes it possible to reconstruct the steps towards social complexity, unravelling how social systems originate and are maintained. Our research on Egernia is funded by a grant from the Australian Research Council.

 

If you want to know more:

While, G.M., Chapple, D.G., Gardner, M.G., Uller, T. & Whiting, M.J. 2015. Egernia lizards. Current Biology 25:R593-595

While, G.M., Uller, T., Bordogna, G. & Wapstra, E. Promiscuity resolves constraints imposed by population viscosity. Molecular Ecology 23: 721-732

While, G. M., Uller, T. & Wapstra, E. 2009. Family conflict and the evolution of sociality in reptiles. Behavioral Ecology 20: 245-250

Extending the Evolutionary Synthesis

The 20th century became known as the century of the gene. The overwhelming focus on genes makes it easy to forget that what is outside of the genome is not only permissive for development, but also instructive. Organisms are inherently flexible and respond to environmental challenges by changing their shape, size, or behaviour. Sometimes such responses can even affect the next generation. The evolutionary implications of developmental plasticity and non-genetic inheritance are poorly understood and highly contested. The fundamental source of contention is if plasticity and non-genetic inheritance are best viewed as adaptive features under genetic control, or if there is value in considering the processes of development and heredity to play a more active role in the origin, spread, and maintenance of adaptations. The latter perspective is increasingly gaining popularity in different calls for ‘extending’ the evolutionary synthesis. Yet, it is unclear how a phenotypic perspective on evolution differs from the gene-centric focus that has been dominant for the last century. Whatever way this debate is headed, building a coherent alternative conceptual framework for phenotypic evolution is a big task that will require biologists with different expertise working together with philosophers and historians of biology.

 

Ultimately, conceptual frameworks should be evaluated on the basis of their ability to generate useful research. Much of the work in our group is therefore motivated by putting our ‘work-in-progress’ version view of an extended evolutionary synthesis to the test. We are always looking for new ways to do so and welcome a diversity of approaches and study systems.

 

For more information, please visit www.extendedevolutionarysynthesis.com

 

If you want to know more:

Laland, K.L., Uller, T, Feldman, M., Sterelny, K., Müller, G.B., Moczek, A., Jablonka, E. & Odling-Smee, J. The extended evolutionary synthesis: its structure, core assumptions, and predictions. Proceedings of the Royal Society of London 282: 20151019

Laland, K.N., Uller, T., Feldman, M.W., Sterelny, K., Müller, G.B., Moczek, A., Jablonka, E. & Odling-Smee, J. 2014. Does evolutionary theory need a rethink? Nature 514: 162-165

Uller, T. & Helanterä, H. Heredity in evolutionary theory. In Challenges to Evolutionary Biology: Development and Heredity (eds. P. Huneman & D. Walsh), Oxford University Press, forthcoming

Laland, K.N., Sterelny, K., Odling-Smee, J., Hoppitt, W. & Uller, T. 2011. Cause and effect in biology revisited: Is Mayr’s proximate-ultimate distinction still useful? Science 334:1512-1516