Rapid evolution of reproductive isolation in newly allopatric invasive populations.

Overview

Invasive populations are ideal model systems to understand the early stages of allopatric speciation, a keystone concept of evolutionary biology (1). Divergent selection to different environments can drive to reproductive isolation and, eventually, speciation (2). The annual, Centaurea solstitialis, (yellow starthistle) is an ideal system to study selection and speciation during a biological invasion. It is native from Eurasia, and invasive in Australia and the Americas (3). It developed different sets of local adaptations to different regions, including some degree of reproductive isolation (1,3-6). The fundamental research undertaken in this PhD project, will address the emergence and maintenance of reproductive isolation in yellow starthistle, and investigate how the balance of selective or neutral processes can lead to incipient speciation in a new allopatric range. This research will contribute substantially to our understanding of how biodiversity is generated and maintained , as well as establishing the likely impacts of invasive populations on biodiversity.

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Image Captions

Map from Global Biodiversity Information Facility gbif.org showing distribution of Yellow Starthistle (pictured on right) in yellow and orange. Sampled regions are marked with red points and approximate native range is indicated with blue ellipse. Main figure: each point is a sample individual coloured according to region plotted according to genetic distance from all other samples. Images reproduced with permission from Irimia (2020) PhD thesis, Coimbra University, Portugal

Methodology

This project builds on an established research collaboration involving the first supervisor at Durham (7). Seed samples representing both the native range (Turkey and Spain) and the neo-allopatric range (Argentina, Chile, California, and Australia) were collected. Plants were grown under common garden conditions and intra- and inter-regional crosses were performed among plants from each region as well as to quantify reproductive isolation between regions (8). Genotyping by sequencing was performed to investigate population genetic structure (4). The next F1 generation of within and between region crossed individuals were then grown under common garden conditions to measure the trait inheritance and differentiation. More genotyping by sequencing data was collected and quantitative trait locus analysis to measure the genetic control of trait and reproductive isolation is underway. Further crosses were performed so that there are now a unique F2 generation resources of intra- and inter-regional crossed seed available for study that have taken years to develop. Studying the F2 generation will allow observation of more recombination and segregation between parental genomes originating in different regions leading to greater sensitivity and precision in determining the quantitative genetic architecture of reproductive isolation and invasive traits. With these unique resources, we will be able to study the worldwide geographic mosaic of local adaptation and reproductive isolation in this invasive species.
The genetic architecture of quantitative trait variation can give insights into its evolutionary origins; it will be critically important to assess the relative importance of chance genetic drift versus selection. For example, simple genetic control by few loci of major effect and acting in the same direction indicate strong recent selection while a shared genetic basis between traits indicate constraints on the independent evolution of those traits. The genetic basis of emerging RI might either be due to fixation by drift of genomic incompatibilities between regions or a pleiotropic by-product of selection in the form of associations with locally adapted traits. This aspect of the study will develop genetic markers associated with important invasive traits to allow monitoring of invasive threats for early and targeted management interventions as well as providing genetic tools for more detailed studies of the key genes involved.

Project Timeline

Year 1

Grow up F2 plants under common garden conditions and measurement of traits related to invasiveness. Perform controlled crosses between individuals derived from similar and different within-region crosses to measure inter-regional reproductive isolation and to generate F3 generation research resources. Collect dried leaf tissue for genetic analysis.

Year 2

Extract DNA and perform genotyping by sequencing. Initiate bioinformatics analysis to extract genotypes and build genetic maps and perform quantitative genetics analysis to determine the combined genetic architecture of reproductive isolation and invasive traits.. Grow up additional F2 plants as required to reinforce sampling gaps identified from Year 1 with suitable controls.

Year 3

Complete additional genotyping by sequencing as necessary to reinforce data analysis. Interpret results and prepare manuscripts. Long-read sequencing of genomic regions of particular interest and identification of F3 individuals to grow up and perform crossing experiments that will allow fine mapping.

Year 3.5

Publish manuscripts and present results at an international conference in the field of evolutionary biology.

Training
& Skills

This project will provide a student with a comprehensive practical and theoretical training in the field of evolutionary plant biology including quantitative genetics and bioinformatics skills. More generally, the project will provide a range of practical skills to continue in scientific research or enter a related industrial sector requiring skills of data acquisition and their analysis and interpretation.

References & further reading

1. Montesinos D, Santiago G, Callaway RM (2012). Neo-allopatry and rapid reproductive isolation. Am Nat. 180:529–33. doi:10.1086/667585
2. Funk DJ, Nosil P, Etges WJ (2006). Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. PNAS 103:3209–13. doi:10.1073/pnas.0508653103
3. Hierro JL, Özkan E, Khetsuriani L, Diaconu A, Török K, Montesinos D, Andonian K, Kikodze D, Janoian L, Villarreal D, Estanga-Mollica ME, Callaway RM (2009). Germination responses of an invasive species in native and non-native ranges. Oikos 118:529-538. 10.1111/j.1600-0706.2009.17283.x
4. Irimia RE, Montesinos D, Chaturvedi A, Sanders I, Hierro JL, Sotes G, Lohengrin A, Cavieres LA, Eren Ö, Lortie CJ, French K, Callaway RM, Brennan AC. Evolution of reproductive and defense traits facilitate rapid weed invasion despite little genetic differentiation. Submitted to New Phytologist
5. Graebner RC, Callaway RM, Montesinos D (2012). Invasive species grows faster competes better and shows greater evolution toward increased seed size and growth than exotic non- invasive congeners. Plant Ecology 213:545-553. 10.1007/s11258-012-0020-x
6. Garcia Y, Callaway RM, Diaconu A, Montesinos D (2013). Invasive and non-invasive congeners show similar trait shifts between their same native and non-native ranges. PlosOne:8(e82281). 10.1371/journal.pone.0082281
7. Irimia RE (2020) Invasive species: ecological and genomic approaches towards understanding local adaptation and early stages of allopatric speciation. PhD thesis. Coimbra University, Portugal.
8. Irimia RE, Hierro JL, Branco S, Sotes G, Cavieres LA, Eren Ö, Lortie CJ, French K, Callaway RM, Montesinos D. Experimental admixture between neo-allopatric regions of an invasive plant yields a global mosaic of reproductive incompatibilities and heterosis. Submitted.

Further Information

Contact: Dr Adrian Brennan, a.c.brennan@durham.ac.uk

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