A transition to selfing can be beneficial when mating partners are scarce, for example, due to ploidy changes or at species range edges. Here we explain how self-compatibility evolved in diploid SiberianArabidopsis lyrata, and how it contributed to the establishment of allotetraploidA. kamchatica. First, we provide chromosome-level genome assemblies for two self-fertilizing diploidA. lyrataaccessions, one from North America and one from Siberia, including a fully assembled S-locus for the latter. We then propose a sequence of events leading to the loss of self-incompatibility in SiberianA. lyrata, date this independent transition to ~90 Kya, and infer evolutionary relationships between Siberian and North AmericanA. lyrata, showing an independent transition to selfing in Siberia. Finally, we provide evidence that this selfing SiberianA. lyratalineage contributed to the formation of the allotetraploidA. kamchaticaand propose that the selfing of the latter is mediated by the loss-of-function mutation in a dominant S-allele inherited fromA. lyrata.

A transition to selfing can be beneficial when mating partners are scarce, for example, due to ploidy changes or at species range edges. Here, we explain how self-compatibility evolved in diploid Siberian Arabidopsis lyrata, and how it contributed to the establishment of allotetraploid Arabidopsis kamchatica. First, we provide chromosome-level genome assemblies for two self-fertilizing diploid A. lyrata accessions, one from North America and one from Siberia, including a fully assembled S-locus for the latter. We then propose a sequence of events leading to the loss of self-incompatibility in Siberian A. lyrata, date this independent transition to ∼90 Kya, and infer evolutionary relationships between Siberian and North American A. lyrata, showing an independent transition to selfing in Siberia. Finally, we provide evidence that this selfing Siberian A. lyrata lineage contributed to the formation of the allotetraploid A. kamchatica and propose that the selfing of the latter is mediated by the loss-of-function mutation in a dominant S-allele inherited from A. lyrata.

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Seagrasses comprise the only submerged marine angiosperms, a feat of adaptation from three independent freshwater lineages within the Alismatales. These three parallel lineages offer the unique opportunity to study convergent versus lineage-specific adaptation to a fully marine lifestyle. Here, we present chromosome-level genome assemblies from a representative species of each of the seagrass lineages -Posidonia oceanica(Posidoniaceae),Cymodocea nodosa(Cymodoceaceae), andThalassia testudinum(Hydrocharitaceae)-along with an improved assembly forZostera marina(Zosteraceae). We also include a draft genome ofPotamogeton acutifolius, a representative of Potamogetonaceae, the freshwater sister lineage to the Zosteraceae. Genome analysis reveals that all seagrasses share an ancient whole genome triplication (WGT) event, dating to the early evolution of the Alismatales. An additional whole genome duplication (WGD) event was uncovered forC. nodosaandP. acutifolius. Dating of ancient WGDs and more recent bursts of transposable elements correlate well with major geological and recent climatic events, supporting their role as rapid generators of genetic variation. Comparative analysis of selected gene families suggests that the transition from the submerged-freshwater to submerged-marine environment did not require revolutionary changes. Major gene losses related to, e.g., stomata, volatiles, defense, and lignification, are likely a consequence of the submerged lifestyle rather than the cause (‘use it or lose it’). Likewise, genes, often retained from the WGD and WGT, were co-opted for functions requiring the alignment of many small adaptations (‘tweaking’), e.g., osmoregulation, salinity, light capture, carbon acquisition, and temperature. Our ability to manage and conserve seagrass ecosystems depends on our understanding of the fundamental processes underpinning their resilience. These new genomes will accelerate functional studies and are expected to contribute to transformative solutions — as continuing worldwide losses of the ‘savannas of the sea’ are of major concern in times of climate change and loss of biodiversity.

Summary/AbstractWhole-genome duplications yield varied chromosomal pairing patterns, ranging from strictly bivalent to multivalent, resulting in disomic and polysomic inheritance modes. In the bivalent case, homeologous chromosomes form pairs, where in a multivalent pattern all copies are homologous and are therefore free to pair and recombine. As sufficient sequencing data is more readily available than high-quality cytological assessments of meiotic behavior or population genetic assessment of allelic segregation, especially for non-model organisms, here we describe two bioinformatics approaches to infer origins and inheritance modes of polyploids using short-read sequencing data. The first approach is based on distributions of allelic read depth at the heterozygous sites within an individual, as the expectations of such distributions are different for disomic and polysomic inheritance modes. The second approach is more laborious and based on a phylogenetic assessment of partially phased haplotypes of a polyploid in comparison to the closest diploid relatives. We discuss the sources of deviations from expected inheritance patterns, advantages and pitfalls of both methods, effects of mating types on the performance of the methods, and possible future developments.