Snapdragon Speciation

Ever since Charles Darwin wrote On The Origin of Species, understanding how new species are generated (speciation) and how genetic barriers between species are maintained remains an unanswered question in evolutionary biology. Central to understanding the process of speciation is identifying the genetic differences involved, how they interact to influence fitness (reproductive success) and how they affect patterns of gene flow (gene exchange) along chromosomes and genomes. Hybrid zones are powerful systems for studying speciation, providing natural laboratories where divergent populations interbreed and produce individuals of mixed ancestry. Here variation in hybrid zones enables an assessment of the link between genotype (genes), phenotype (traits) and fitness, which is essential for understanding selection and barriers to gene flow. We use hybrid zones between two sub-species of Antirrhinum majus (snapdragons) to quantify how interactions among genes shape fitness variation and the strength of genetic barriers. This system is ideal to assess these questions as there are a number of known genes that control flower colour patterns that differ between the sub-species and are under selection due to pollinator preferences. These two sub- species have evolved two alternative adaptive phenotypes that are signposts for pollinators: A. majus pseudomajus is magenta coloured with a patch of yellow at the flower entry point and A. majus striatum is yellow with magenta veins at the entrance of the flower. This raises the question: how are these alternative adaptive phenotypes maintained in the face of gene flow? To answer this question, we will integrate approaches that assess how independent genomic regions controlling colour differences relate to fitness variation within generations with spatial approaches (clines) that quantify barriers to gene flow across generations. Bridging the gap between different evolutionary time-scales has been a long-standing challenge in the field of evolutionary biology. We will measure individual fitness and obtain genome-wide DNA sequences in order to directly estimate selection and compare this to indirect estimates from the properties (steepness) of spatial clines. This will be done across multiple hybrid zones, which provides a means of testing the generality of these processes and distinguishing the genetic signatures of selection from random background noise in the genome. These questions require the development of new techniques to identify genetic barriers in genomic data, which will extend the availability of tools to analyse genome wide data, both here and for other study organisms. In summary, combining these approaches provides a novel way of connecting evolutionary processes acting over different timescales, thereby providing insight into genetic barriers and the signatures they leave behind in genomic data.

In the eastern Pyrenees, two subspecies of snapdragon (Antirrhinum majus) meet and hybridise: the population shifts from plants with yellow to magenta flowers over a kilometre. Such "hybrid zones" form natural laboratories in which we can study the genetic basis of reproductive isolation, and the processes that can ultimately lead to the origin of new species. In our long-term study, we have characterised 36,000 plants for 100 genetic polymorphisms. This allows us to determine the relationships between individuals, giving direct estimates of fitness and of the movement of seed and pollen. These show that the sharp transition is maintained, despite the random mixing of the two populations, because hybrids and rarer flower types produce fewer offspring. In this FWF project, we made an intensive survey over two seasons, following each of ~800 plants for 90 days. We also sequenced the whole genome using a new method ('haplotagging'), developed by our collaborator (Frank Chan, Univ. Groningen). This will allow us to measure total fitness, and to attribute it to specific genetic variants. in a genome-wide association study (GWAS). We have also grown up and genotyped seedlings from fruits harvested from these intensively-studied plants, which will allow us to determine the relative success of different plants as fathers. Altogether, this is (to our knowledge) the most intensive study of a natural plant population, and will give unique information about variation in fitness in nature, and about the evolution of reproductive isolation.