Associations between genomic ancestry, genome size and capitula morphology in the invasive meadow knapweed hybrid complex (Centaurea ×moncktonii) in eastern North America

Authors: LACHMUTH, SUSANNE - Martin Luther University; MOLOFSKY, JANE - University Of Vermont; Milbrath, Lindsey; SUDA, JAN - Charles University, Czech Republic; KELLER, STEPHEN - University Of Vermont

Submitted to: AoBP (Annals of Botany PLANTS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/15/2019
Publication Date: 8/23/2019
Citation: Lachmuth, S., Molofsky, J., Milbrath, L.R., Suda, J., Keller, S.R. 2019. Associations between genomic ancestry, genome size and capitula morphology in the invasive meadow knapweed hybrid complex (Centaurea ×moncktonii) in eastern North America. AoBP (Annals of Botany PLANTS). 11(5). https://doi.org/10.1093/aobpla/plz055.
DOI: https://doi.org/10.1093/aobpla/plz055

Interpretive Summary: Meadow knapweed is a hybrid of black and brown knapweeds and is becoming increasingly problematic in the northeastern U.S. and elsewhere. This hybrid weed complex is not well studied in either North America or its native European range. Hybridization is hypothesized to promote invasiveness in plants. Genomic and morphological characteristics were determined from 20 knapweed populations from New York and Vermont to determine ancestral relationships and their genetic diversity. Three distinct lineages were identified, two that are similar, but not necessarily identical, to the parental black and brown knapweeds and one that represents a mixture of hybrid meadow knapweeds. As expected, the meadow knapweed populations were variable in genomic and morphological characteristics. Backcrossing is continuing between different hybrids and with the parental forms. This study provides a foundation for further work aimed at addressing the impact of hybridization and changes in plant genomes on promoting invasion success.

Technical Abstract: Plant invasions are prime opportunities for studying hybridization and the nature of species boundaries, but hybrids also complicate the taxonomic treatment and management of introduced taxa. In this study, we use population genomics to estimate the extent of genomic admixture and test for its association with morphology and genome size in a hybrid complex of knapweeds invasive to North America: meadow knapweed (Centaurea ×moncktonii) and its parental species (C. jacea and C. nigra). We sampled 20 populations from each of ten locations in New York and Vermont, USA, and used genotyping-by-sequencing to identify single nucleotide polymorphisms in order to estimate genome-wide ancestry and classify individuals into hybrid genotype classes. We then tested for association between degree of genomic introgression and variation in some diagnostic traits of the parental taxa, namely capitula floral traits and monoploid genome size. Genomic clustering revealed two clearly-defined lineages with minimal admixture, and also many admixed individuals displaying a continuous gradation of introgression. Hybrid genotype assignments revealed many advanced generation backcrosses, suggesting introgression has been extensive and unimpeded by strong reproductive barriers between taxa. Variation in capitula traits between the unadmixed presumed parental lineages graded into nearly continuous, and in some cases transgressive, segregation among introgressed hybrids. Genome size was also divergent between lineages, although advanced generation hybrids had comparably smaller genomes. Our study demonstrates deep introgression between the porous genomes of a hybrid invasive species complex. In addition to strong associations among genomic ancestry, genome size, and morphology, hybrids expressed greater variation in capitula traits and genome size, indicating transgressive segregation, as well as a bias towards smaller genomes, possibly due to genomic downsizing. Future studies will apply these results to experimentally test how introgression, transgressive segregation, and genome size reduction interact to confer invasiveness.