Recurrent allopolyploidy and its implications for conservation in vascular plants: a commentary on ‘Population genomics of the Isoetes appalachiana (Isoetaceae) complex supports a “diploids-first” approach to conservation’

The evolutionary dynamics of allopolyploidy in plant species has captivated researchers for decades. This intricate process involves whole genome duplication associated with the fusion of genomes from plants originating in different lineages. Polyploidy overall (auto- and allopolyploidy) appears to be less of an exception and more of a common process in most plant lineages. Recent estimates indicate that a substantial proportion (35–50 % – Wood et al., 2009; Van de Peer et al., 2017) of vascular plants are products of recent polyploidy events (Alix et al., 2017; Van de Peer et al., 2017). Traditionally viewed as evolutionary dead ends, they are now recognized as players in the process of speciation, possibly contributing to rapid reproductive isolation and influencing the ecological and evolutionary landscape (Van de Peer et al., 2020). While polyploidy can adversely affect fertility and survival, it can simultaneously enhance genetic variation, potentially conferring increased tolerance to a broad spectrum of ecological challenges. Genome-scale analyses spanning various lineages have shown the relevance and significance of polyploidy as a pivotal process both historically (palaeopolyploidy) and presently (neopolyploidy) in shaping diversity and driving innovation among land plants.

The study by Wickell et al. (2023) in this issue of the Annals of Botany illuminates the recurrent formation and limited gene flow of allopolyploid lineages in the lycophyte Isoetes appalachiana, an aquatic species of the eastern USA. The study unravels its intricate genomic history through high-throughput sequencing and a read-phasing approach, adding to the broader discussion on polyploidy in plant evolution. Their results shed light on the recurrent, but not reciprocal, formation of allopolyploids in I. appalachiana. Despite the genomic complexity and potential for long-range dispersal in Isoetes, the research reveals surprisingly limited evidence of admixture among geographically distinct populations, raising questions about the frequency of such events and potential postzygotic barriers.

Beyond offering new insights into the history of recurrent polyploidization in Isoetes, Wickell et al. (2023) have raised an important discussion about prioritization in the conservation and management of rare species belonging to this genus. According to the authors, conservation efforts might be directed towards preserving diploids, as polyploids are both ephemeral and isolated from their progenitors. Although this might be true for the I. appalachiana complex, it cannot be generally assumed for other multiploid plant lineages. Studies have often shown that polyploids may be long-established species exhibiting increased adaptive potential in stressful environments (Van de Peer et al., 2020), which probably represents an advantage in the climate-changing present-day world. Moreover, growing evidence shows that ploidy barriers do not impede gene flow, which might have important consequences for adaptation via introgression. Preserving polyploid lineages is, thus, of special interest as they may be more likely to represent diverse and adaptable evolutionary lineages (see Schmickl and Yant, 2021).

The methodological contributions made by Wickell et al. (2023) are also noteworthy. While high-throughput sequencing technologies are becoming increasingly accessible, there is still a limited set of comprehensive tools and specific software to perform genomic analysis of polyploid systems (Meirmans et al., 2018). Methodological issues, such as determining allelic dosage, distinguishing paralogous sequences and phasing the subgenomes, remain to be fully addressed. Despite the considerable efforts made in the last few years (e.g. Brandrud et al., 2020; Bloesch et al., 2022), allocating the high volume of data generated by high-throughput sequencing into the different parental subgenomes is particularly challenging. Wickell et al. (2023) built a polyploid pseudoreference using reads from both diploid parental species, then retained the reads from the polyploid that preferentially aligned to each diploid from the pseudoreference so that they could be used as diploid inputs for subsequent analyses at homoeologous loci. This approach can be replicated in other study systems unless general information on the identity of the diploid progenitors is lacking, or no genome assembly is available as a reference for raw read alignment.

By combining RAD sequencing and genome skimming, Wickell et al. (2023) acquired population-level data from a reduced representation of the genome of the studied species. These methods are suitable for inferring phylogenetic relationships and population structure, offering a particularly innovative and cost-effective solution for non-model species with large genome sizes. Given the notably large genomes of ferns and lycophytes (Wang et al., 2022) and the putative occurrence of single species originating from multiple independent events of allopolyploidization, employing a reduced representation of the genome for a larger number of samples may be preferable to sequencing the whole genomes of only a few individuals or populations. However, reduced representation methods must provide sufficient loci, once allopolyploids tend to become diploidized over time, resulting in the loss of parts from each sub-genome.

By unravelling the complex genomic interactions within Isoetes, Wickell et al. (2023) have not only contributed to our understanding of this enigmatic group but also prompted a re-evaluation of conservation strategies considering the evolutionary dynamics at play. Their study marks a significant step forward in our understanding of plant polyploidy, urging researchers to explore the complex interplay of hybridization, polyploidization and speciation in the broader context of vascular plants. The association of whole genome duplications with pivotal periods of global climatic and geological change or mass extinctions suggests a non-random pattern in their long-term survival (Van de Peer et al., 2017, 2020). The resulting lineages, often formed during major environmental transitions, may exhibit distinctive phenotypes and explore diverse adaptations from their parental genomes, occupying different ecological niches. Allopolyploidy, specifically, stands out as a mechanism capable of generating new lineages and fostering variability through processes such as introgression. It is high time to acknowledge and include the recurrent formation of polyploid lineages, a key factor in the evolutionary success of vascular plants, in the biological conservation stage.

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