Genomics and phylogenetics inform a species recovery plan for a threatened allopolyploid plant

Abstract In the USA, 944 plant taxa are listed as threatened or endangered under the Endangered Species Act. Brassicaceae is the fourth most threatened family with 41 listed species. This study focuses on slickspot peppergrass (Lepidium papilliferum), a threatened Brassicaceae endemic to south-western Idaho that is experiencing significant population decline and reduced fecundity. Our goal is to support the establishment of a breeding and genetic rescue programme to restore populations of this species by addressing the following objectives: (i) confirm its genomic origin, (ii) investigate the importance of ancestral hybridization on its origin, (iii) propose a phylogeographic hypothesis to inform its restoration, and (iv) offer conservation and restoration guidelines. We sampled 44 L. papilliferum individuals from 27 element occurrences (populations) across three landscape management regions, as well as 16 individuals from closely related species. Using Illumina sequencing, we assessed genome size and heterozygosity, and conducted phylogenetic and genetic clustering analyses on nuclear and plastome data. Results showed that L. papilliferum has an allopolyploid origin, with genome size variation and genotype frequencies supporting segmental allopolyploidization. Genomic discordance suggested the occurrence of ancestral hybridization events. Nuclear phylogenetic analysis confirmed the species’ monophyly, possibly because of genetic isolation driven by ecological speciation. We used genetic groups to redefine landscape management regions for the species, offering new boundaries for a forthcoming species recovery plan. This research provides essential genetic insights to inform the restoration of slickspot peppergrass populations and guide conservation efforts.