Sex-linked loci, sexual specialization and local adaptation in Mercurialis annua complex (2013-2014) – FP7-PEOPLE-2012-IEF (Marie Curie Intra-European Fellowship)
The sexual and genetic systems of a plant species directly regulate how genes are transmitted across generations. Accordingly, their study is of central importance to understand plant evolution. Populations of widespread plants normally have higher fitness at their home site than in other parts of the range. However, the genetic and molecular mechanisms underlying local adaptation are not well understood yet. How do plant populations adapt to a rapidly changing world? Why and how separate sexes evolve and are maintained in plants? What are the consequences of broad variation in sexual systems for plant survival at different spatial scales (local, widerange)? This Senior Marie Curie project conduct innovative and multidisciplinary research, using state-of-the-art sequencing technology, to investigate how natural selection brings about local adaptation in plant populations with contrasting sexual (separate vs. combined sexes) and genetic (diploidy vs. polyploidy) systems. To address these questions, we are studying the ecological genomics of local adaptation in the Mercurialis annua s.l. species complex. This species complex shows an unusually broad variation in its sexual and genetic systems, as well as large phenotypic geographical variation, thus providing an outstanding model to study, at the genomic level, the role of mating and genetic factors on local adaptation.
The expression, selection and evolution of combined vs. separate sexes in an annual plant (2012-2015) – Swiss National Science Foundation
Plants present a startling array of sexual systems that directly regulate how genes throughout the genome are transmitted to the next generation. A particularly clear contrast is between plants that are hermaphroditic (i.e., that have combined sexes), and plants that are dioecious (i.e., that have separate sexes). Most flowering plants are hermaphrodites, but evolutionary transitions between hermaphroditism and dioecy have been frequent. What forces drive transitions from hermaphroditism to dioecy has been the focus of a great deal of theorising. Hypotheses fall broadly into two classes: the ‘inbreeding avoidance hypothesis’ that dioecy evolves as an outcrossing mechanism, principally to avoid the detrimental costs of self-fertilisation; and the ‘sexual specialisation hypothesis’ that dioecy evolves in response to selection for specialisation in the allocation of resources to male vs. female functions, e.g., because of advantages of specialised inflorescences, morphology, physiology, etc., for males vs. females. Of these two hypotheses, the first has received more empirical attention than the second, probably because it is not easy to measure the direct and indirect fitness benefits of being a gender specialist vs. generalist, particularly for male function.
In this project, we propose to use a system that has been developed as an outstanding model for the study of plant sex allocation (reproductive investment into male vs. female functions) and sexual-system transitions to address several questions mainly relevant to the sexual specialisation hypothesis: What are the fitness benefits of sexual specialisation, particularly in terms of size and inflorescence architecture? How do specialised inflorescences evolve within a genus, what is the genetic architecture of inflorescence variation within a species, and how does this affect fitness? How does selection for sexual specialisation operate in a context in which individuals compete for both mates and limited resources, particularly when individuals competing with one another for resources share common evolutionary interests in terms of co-parentage? How does sexual specialisation in sex allocation affect herbivory, and how does sex-differential herbivory in turn affect fitness? When separate sexes do evolve, how is their sex determined, and are the same (genetic) mechanisms re-adopted when separate sexes are lost and then regained? In cases where the local environment affects sex expression, what environmental cues are used. When the separation of the sexes breaks down, such that hermaphroditism evolves from dioecy, what selective factors are responsible? In particular, is there any direct evidence that selection for reproductive assurance can lead to the evolution of hermaphroditism from dioecy? Finally, what factors influence the expression and evolution of hermaphroditic sex allocation, i.e., the division of resources between male and female functions?
We propose to address these questions using a combination of comparative (morphological and genomic) and experimental approaches (experimental evolution and mating-system manipulation) using the clade of wind-pollinated annual species in the genus Mercurialis (Euphorbiaceae), which shows remarkable variation in the distribution of gender and sex allocation among species and populations within species. A particularly novel aspect of our application is the plan to use natural selection in situations where the context of competition for mates and/or resources has been manipulated to expose the factors responsible for phenotypic evolution of sex allocation and sexual system. Another novel aspect is the proposal to use high throughput sequencing to uncover new sex-linked markers in dioecious species, and to trace these sex-linked markers through a clade in which separate sexes have come and gone more than once.
The project builds on more than a decade of intensive study of one of the species in the annual Mercurialis clade, M. annua, for which a great deal is now known about the species’ phylogenetic and phylogeographic histories, the genetic architecture of sex allocation (including responsiveness to artificial and natural selection), natural patterns of sex allocation at a wide range of spatial scales, and the expression of gender and sexual dimorphism under various environmental conditions. Diploid-acting microsatellites have recently been developed for M. annua using a novel approach that overcomes the difficulties of polyploidy, and both a reference transcriptome and the genome of diploid M. annua have just been sequenced. This previous work places us in a strong position to address the important questions outlined above using novel approaches in a well-characterised ecological genetic model.
The evolutionary genomics of recombining sex chromosomes (2014-2017) – Swiss National Science Foundation (Sinergia program)
Our project aims at integrating innovative theoretical and conceptual approaches with genetic/genomic investigations of nascent sex chromosomes. On one hand, we will develop evolutionary models and statistical procedures aimed at formalizing the dynamic view of sex-chromosome evolution that emerges from recent studies of non-model organisms. On the other hand, these models and procedures will be calibrated and tested with genetic/genomic data gathered from two highly divergent lineages (angiosperms and amphibians).
Our evolutionary models will focus on two main questions: i) Why do some chromosomes evolve suppressed recombination and others not? And ii) What drives turnovers in sex determination systems? To do so, we will examine the interplay between sex-determination genes, sexually antagonistic genes, deleterious mutations and recombination on the dynamics and evolution of sex chromosomes. We will build on the conceptual frameworks, analytical methods and individual-based simulations already developed in our labs (e.g. van Doorn & Kirkpatrick 2007, 2010; Grossen et al. 2011; Blaser et al. 2012).
Statistical procedures will characterize processes of molecular evolution in recombining sex chromosomes. We aim to predict patterns of neutral genetic variation expected on sex chromosomes experiencing deleterious/beneficial mutations and recombination. One of the goals is to identify signatures of sexually antagonistic selection in recombining sex chromosomes. We will also build on conceptual and analytical frameworks (such as Approximate Bayesian computations) already developed in our labs (e.g. Guerrero et al. 2012).
Empirical calibration and tests of predictions stemming from the above models and procedures will focus on a group of plants (Mercurialis spp.) and amphibians (Rana spp.) identified for their labile sex determination systems and recombining sex chromosomes. For both group of species we will combine RAD-tag sequencing and transcriptome analyses with family pedigrees to measure X-Y differentiation and identify signatures of selective pressures along the recombining chromosomes. This will be done for several species from each radiation that differ in sex determination systems.