Mating systems and genetic diversity in Arabidopsis lyrata
Lead Research Organisation:
University of Glasgow
Department Name: Environmental and Evolutionary Biology
Abstract
The proposed research is concerned with evaluating how the mating 'decisions' that plants make affect their potential to respond to environmental change, as a result of changes in genetic diversity resulting from different levels of inbreeding. This project will address this question by examining naturally occurring populations of a species that is normally outcrossing (i.e., is only able to breed with unrelated individuals), but for which populations have been identified that have experienced a change in the genetic machinery required to maintain this mating strategy. The study will examine variation in 1) genes that are directly involved in controlling rates of outcrossing; 2) genes that are in physical proximity to these gene regions; and 3) unrelated reference loci that can be used to test population genetics models about changes in demographic attributes of populations in relation to breeding systems. The tied studentship will test hypotheses about when the shift in mating system occurred in relation to post-glacial colonization to their current distribution area and whether loss of outcrossing mechanisms is a heritable trait. Since the plants used in this study are restricted to habitats that have been fragmented as a result of human population growth, the study could have implications for predicting how changes in breeding strategies will influence the ability of populations to adapt to changes in population size or restriction of migration between populations as a result of human activities.
Publications
Foxe JP
(2010)
Reconstructing origins of loss of self-incompatibility and selfing in North American Arabidopsis lyrata: a population genetic context.
in Evolution; international journal of organic evolution
Haudry A
(2012)
Disentangling the effects of breakdown of self-incompatibility and transition to selfing in North American Arabidopsis lyrata.
in Molecular ecology
Hoebe PN
(2011)
The effect of mating system on growth of Arabidopsis lyrata in response to inoculation with the biotrophic parasite Albugo candida.
in Journal of evolutionary biology
Hoebe PN
(2009)
Multiple losses of self-incompatibility in North-American Arabidopsis lyrata?: phylogeographic context and population genetic consequences.
in Molecular ecology
Mable B
(2018)
Adding Complexity to Complexity: Gene Family Evolution in Polyploids
in Frontiers in Ecology and Evolution
Mable BK
(2017)
What causes mating system shifts in plants? Arabidopsis lyrata as a case study.
in Heredity
Mable BK
(2008)
Genetic causes and consequences of the breakdown of self-incompatibility: case studies in the Brassicaceae.
in Genetics research
Stift M
(2010)
Inheritance in tetraploid yeast revisited: segregation patterns and statistical power under different inheritance models.
in Journal of evolutionary biology
Tedder A
(2011)
Sporophytic self-incompatibility genes and mating system variation in Arabis alpina.
in Annals of botany
| Description | Training: The objectives of this project were to investigate the causes and consequences of mating system variation in Arabidopsis lyrata, which is a long-lived perennial that is outcrossing throughout most of its range. This project directly funded one postdoc (Marc Stift), one PhD student (Andrew Tedder) and a 50% technician (Aileen Adam) but another PhD student (Peter Hoebe) and two other postdocs (Hong-Guang Zha and Annabelle Haudry) funded from other sources also contributed to the project. A succession of undergraduate students (honours projects and vacation studentships) also contributed to data collection and were trained in association with the grant. In addition, we collaborated closely with researchers at the University of Toronto (Stephen Wright and his PhD student John Paul Foxe). The project therefore provided a valuable opportunity for participants to learn to work as part of a team and to write collaborative papers, as well as maintaining responsibility for their own individual aspects of the research. Both PhD students and the postdoc directly funded on the project successfully obtained postdoctoral research positions before the end of their funding and are continuing in related research areas. Outcomes and Achievements: Specifically, this project proposed to compare changes in diversity in: 1) genes that are directly involved in determining specificity of the self-incompatibility (SI) reaction that maintains outcrossing (i.e. at the S-locus) and are thus under strong balancing selection to maintain diversity; 2) genes that are physically linked to these genes in a region of low recombination and are thus likely to hitchhike along with the selected region; and 3) reference loci that are unrelated to the SI phenotype and located on different chromosomes, with the goal of increasing understanding of the selective pressures that act to maintain functional SI systems and the consequences of loss of SI for genes scattered throughout the genome. We focused on samples from 24 populations around the Great Lakes region of eastern North America that vary in the proportion of self-compatible (SC) individuals and in population outcrossing rates. An important finding was that the loss of SI does not lead to a shift to inbreeding in all populations (i.e. some populations that contain a mixture of SI and SC individuals remained highly outcrossing and maintained high levels of individual heterozygosity, suggesting that individuals still outcrossed even though capable of self-fertilizing). Most studies investigating the causes and consequences of shifts in mating systems between species have not considered that this is a two-step process and that different selective forces may be operating. Based on neutral markers (microsatellites, chloroplast DNA and 18 nuclear gene sequences), our data suggested that loss of SI and the shift to inbreeding has occurred in different genetic backgrounds, suggesting that the shift in mating system may have occurred more than once in the process of postglacial expansion to the north of the Great lakes in the last 10,000 years. Although the phylogeographic patterns remains uncertain because our study did not include samples from unglaciated regions to the south, our results have fuelled interest for further study by other researchers and has contributed to attainment of a new NERC project for the PI. Nevertheless, multiple losses of SI goes against the dogma that it should be difficult for highly outcrossing species to shift to inbreeding, due to the high genetic loads accumulated after a long history of outcrossing. We found that even the outcrossing North American populations did not show the high levels of inbreeding depression (ibd) found in European populations. It is possible that a bottleneck associated with long-distance migration of North American populations from Europe (which has been suggested by other researchers and supported by our data, based on found lower levels of genetic diversity in North American vs European populations) has resulted in purging of the genetic load. Although we were unable to obtain full genotypes at the S-locus (because of the high levels of diversity and similarity to other members of the gene family) for all individuals from the outcrossing populations (we have obtained an NBAF small projects grant to complete this using tagged amplicon sequencing using 454), we did find that inbreeding populations had only a few alleles, with the phylogeographic distribution consistent with a bottleneck rather than selection leading to the shift in mating system, which contrasts with predictions of selective sweeps proposed for other species. Finally, our work on genes flanking the S-locus suggested that tight linkage and lack of recombination are maintained even in inbreeding populations, suggesting either that the shift to inbreeding has been too recent to observe a change or that the S-locus maintains some functionality, even after loss of SI. Together, our results emphasize that there should be a shift in thinking about the processes regulating mating system variation. Update: February 2016 Part of this work that was left incomplete after various postdoctoral fellows left has now been included in a publication that was invited for a submission for a Special Issue of Heredity, to commemorate the 50th anniversary of the Population Genetics group. Mating system evolution has been of key interest to this community and the data originally collected for this grant have now been combined with next generation sequencing approaches to investigate the genetic causes of the loss of self-incompatibility. This has revealed new insights into the process in a very young transition to inbreeding. The interpretations of this work rely on the classical genetics, traditional cloning and sequencing generated for this grant, combined with this more advanced approach. The work was initiated while I was on fellowship NE/B50094X/1 but the data analysis has finally been completed in February 2016. |
| Exploitation Route | This research has been well-cited and has attracted interest from others interested in mating system evolution. Since shifts from outcrossing to inbreeding are one of the most common transitions in flowering plants, this has very wide implications. Importantly, this was the first extensive study of patterns of geographic variation within species that vary in mating system. Our finding of multiple origins of inbreeding is important because it suggests that the advantages of inbreeding are not considered enough in models of adaptation to changing environments. This has important implications for understanding the impacts of climate change on crop plants, because mating system is a trait often manipulated. |
| Sectors | Agriculture, Food and Drink,Environment |
| URL | http://www.gla.ac.uk/researchinstitutes/bahcm/staff/barbaramable/barbaramable/ |
| Description | Multiple publications have resulted from this research, including studies conducted by other researchers. Findings from this study have also been used to obtain additional grant funding. |
| First Year Of Impact | 2009 |
| Sector | Agriculture, Food and Drink,Environment |
| Title | SRK and flanking gene genotypes for Arabidopsis lyrata |
| Description | Genotypes at the S-related kinase (SRK) gene and associated flanking genes (B70, B80, B120, B160) of Arabidopsis lyrata, comparing patterns of diversity in self-compatible and self-incompatible populations from the Great Lakes region of Eastern North America. |
| Type Of Material | Database/Collection of data |
| Year Produced | 2017 |
| Provided To Others? | Yes |
| Impact | This is the only multi-population survey of genotypes at an important locus under balancing selection, the SRK gene that controls self-incompatibility in Brassicaceae and its associated flanking genes. Importantly, this documents a clear bottleneck in self-compatible populations and provides new insights into the evolutionary processes associated with shifts in mating system. |
| URL | http://dx.doi.org/10.5061/dryad.832t8 |
| Title | Tagged amplicon sequences for the S-locus related kinase gene for Arabidopsis lyrata |
| Description | These data have been deposited to the short read archive (bioproject ID: PRJNA339675). These are Illumina sequences generated using a novel shearing approach to sequence a 900 bp fragment of the S-related kinase gene (SRK) from Arabidopsis lyrata samples from the Great Lakes region of eastern North America. |
| Type Of Material | Database/Collection of data |
| Year Produced | 2017 |
| Provided To Others? | Yes |
| Impact | This is a new methodology that we think will be useful to others. It was developed by the Nerc Biomolecular analysis facility team at the University of Liverpool, to enable amplicon sequencing of large gene fragments (the previous limit was 450 bp). |
| Title | Whole genome sequence pools from self-compatible Arabidopsis lyrata |
| Description | Illumina sequences have been deposited to the short read archive (Bioproject ID: PRJNA339675) from a pool of 10 individuals with a self-compatible phenotype (Arabidopsis lyrata). |
| Type Of Material | Database/Collection of data |
| Year Produced | 2017 |
| Provided To Others? | Yes |
| Impact | These data will be useful for other researchers investigating the genetic basis for loss of self-incompatibility, particularly in plants with a sporophytic system. |