Population genomics of the Isoetes appalachiana (Isoetaceae) complex supports a 'diploids-first' approach to conservation.

Abstract

Allopolyploidy is an important driver of diversification and a key contributor to genetic novelty across the tree of life. However, many studies have questioned the importance of extant polyploid lineages, suggesting that the vast majority may constitute evolutionary 'dead ends'. This has important implications for conservation efforts where polyploids and diploid progenitors often compete for wildlife management resources. Isoetes appalachiana is an allotetraploid that is broadly distributed throughout the eastern USA alongside its diploid progenitors, I. valida and I. engelmannii. As such, this species complex provides an excellent opportunity to investigate the processes that underpin the formation and survival of allopolyploid lineages. Here we utilized RADseq and whole-chloroplast sequencing to unravel the demographic and evolutionary history of hybridization in this widespread species complex. We developed a modified protocol for phasing RADseq loci from an allopolyploid in order to examine each progenitor's genetic contribution independently in a phylogenetic context. Additionally, we conducted population-level analyses to examine genetic diversity and evidence of gene flow within species. Isoetes appalachiana is the product of multiple phylogenetic origins, suggesting that formation and establishment of allopolyploids are common in this group. Hybridization appears to be unidirectional, with I. engelmannii consistently being the maternal progenitor. Additionally, we find that polyploid lineages are genetically isolated, rarely if ever experiencing gene flow between geographically distinct populations. Allopolyploid lineages of I. appalachiana appear to form frequently and experience a high degree of genetic isolation following formation. Thus, our results appear to corroborate the hypothesis that the vast majority of recently formed polyploids may represent evolutionary dead ends. However, this does not necessarily lessen the evolutionary importance or ecological impact of polyploidy per se. Accordingly, we propose a conservation strategy that prioritizes diploid taxa, thus preserving downstream processes that recurrently generate allopolyploid diversity.